The Works of Francis Balfour 2-15
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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.
- The Ovum and Spermatozoon | The Maturation and Impregnation of the Ovum | The Segmentation of the Ovum | Dicyemae and Orthonectidae Dicyema | Porifera | Coelenterata | Platyhelminthes | Rotifera | Mollusca | Polyzoa | Brachiopoda | Chilopoda | Discophora | Gephyrea | Chaetognatha | Nemathelminthes | Tracheata | Crustacea | Pcecilopoda | Echinodermata | Enteropneusta | Bibliography
The Works of Francis Balfour Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.
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Vol II. A Treatise on Comparative Embryology (1885)
CHAPTER XV. Chatognatha, MYZOSTOMEA AND GASTROTRICHA
THE present chapter deals with three small isolated groups, which only resemble each other in that the systematic position of all of them is equally obscure.
The discoveries of Kowalevsky (No. 378) confirmed by Btitschli (No. 376) with reference to the development of Sagitta, though they have not brought us nearer to a knowledge of the systematic position of this remarkable form, are nevertheless of
FIG. 164. THREE STAGES IN THE DEVELOPMENT OF SAGITTA. (A and C after Hiitschli and B after Kowalevsky.) The three embryos are represented in the same positions.
A. The gastrula stage.
li. A succeeding stage in which the primitive archenteron is commencing to be divided into three parts, the two lateral of which are destined to form the body cavity.
C. A later stage in which the mouth involution (/;/) has become continuous with the alimentary tract, and the blastopore has become closed.
m. mouth; al. alimentary canal ; ae. archenteron ; bl.p. blastopore; pv. perivisceral cavity; sf>. splanchnopleuric mesoblast; so. somatopleuric mesoblast ; ge. generative organs.
great value for the more general problems of embryology. The development commences after the eggs are laid. The segmentation is uniform, and a blastosphere, formed of a single layer of columnar cells, is the product of it. An invagination takes place, the opening of which narrows to a blastopore situated at the pole of the embryo opposite that at which the mouth subsequently appears (fig. 164 A). The simple archenteron soon becomes anteriorly divided into three lobes, which communicate freely with the still single cavity behind (fig. 164 B). The two lateral lobes are destined to form the body cavity, and the median lobe the alimentary tract of the adult. An invagination soon arises at the opposite pole of the embryo to the blastopore and forms the mouth and oesophagus (fig. 164 B and C, m).
At the gastrula stage there is formed a paired mass destined to give rise to the generative organs. It arises as a prominence of six cells, projecting from the hypoblast at the anterior pole of the archenteron, and soon separates itself as a mass, or probably a pair of masses, lying freely in the cavity of the archenteron (fig. 164 A. y ge). When the folding of the primitive cavity takes place the generative rudiment is situated at the hind end of the median lobe of the archenteron in the position represented in fig. 164 C, ge.
An elongation of the posterior end of the embryo now takes place, and the embryo becomes coiled up in the egg, and when eventually hatched sufficiently resembles the adult to be recognisable as a young Sagitta.
Before hatching takes place various important changes become manifest. The blastopore disappears after being carried to the ventral surface. The middle section of the trilobed region of the archenteron becomes separated from the unpaired posterior part, and forms a tube, blind behind, but opening in front by the mouth (fig. 165 A, al). It constitutes the permanent alimentary tract, and is formed of a pharyngeal epiblastic invagination, and a posterior hypoblastic section derived from the primitive archenteron. The anus is apparently not formed till comparatively late. After the isolation of the alimentary tract the remainder of the archenteron is formed of two cavities in front, which open freely into a single cavity behind (fig. 165 A). The whole of it constitutes the body cavity and its walls
f/ic mesoblast. The anterior paired part becomes partitioned off into a head section and a trunk section (fig. 165 A and B). The former constitutes a pair of distinct cavities (c.pv) in the head, and the latter two cavities opening freely into the unpaired portion behind. At the junction of the paired cavities with the unpaired cavity are situated the generative organs (ge). The inner wall of each of the paired cavities forms the splanchnopleuric mesoblast, and the outer wall of the whole the somatic mesoblast. The inner walls of the posterior cavities unite above and below the alimentary tract, and form the dorsal and ventral mesenteries, which divide the body cavity into two compartments in the adult. Before the hatching of the embryo takes place this mesentery is continued backwards so as to divide the primitively unpaired caudal part of the body cavity in the same way.
From the somatic mesoblast of the trunk is derived the single layer of longitudinal muscles of Sagitta, and part of the epithelioid lining of the body cavity. The anterior termination of the trunk division of the body cavity is marked in the adult by the mesentery dividing into two laminae, which bend outwards to join the body wall.
The cephalic section of the body cavity seems to atrophy, and its walls to become converted into the complicated system of muscles present in the head of the adult Sagitta.
In the presence of a section of the body cavity in the head the embryo of Sagitta re sembles Lumbricus, Spiders, etc.
The generative rudiment of each side divides into an anterior and a posterior part
In;. [65. Two VIEWS OF A LATE EMBRYO OF SV.ITTA. A. from the dorsal surface. I?, from the tide. (After 15iitschli.)
m. mouth ; al. alimentary canal ; v.g. ventral ganglion (thickening of epiblast) ; rp. epiblast ; c.pv, cephalic section of body cavity; so. somatopleure ; s/>. splanchnopleure ; ,;v. generative
(fig. 165, ge]. The former constitutes the ovary, and is situated in front of the septum dividing the tail from the body ; and the latter, in the caudal region of the trunk, forms the testis.
The nervous system originates from the epiblast. There is a ventral thickening (fig. 165 B, v.g) in the anterior region of the trunk, and a dorsal one in the head. The two are at first continuous, and on becoming separated from the epiblast remain united by thin cords.
The ventral ganglion is far more prominent during embryonic life than in the adult. Its position and early prominence in the embryo perhaps indicate that it is the homologue of the ventral cord of Chaetopoda 1 .
(376) O. Biitschli. "Zur Entwicklungsgeschichte der Sagitta." Zeitschrift f. wiss. Zoo!., Vol. xxni. 1873.
(377) C. Gegenbaur. " Uber die Entwicklung der Sagitta." Abhand. d. naturforschenden Gesellschaft in Halle, 1857.
(378) A. Kowalevsky. " Embryologische Studien an Wiirmern u. Arthropoden." Mem. Acad. Petersbourg, VII. ser., Tom. XVI., No. 12. 1871.
The development of these peculiar parasites on Crinoids has been investigated by Metschnikoff (No. 380), Semper (No. 381), and Graff (No. 379).
The segmentation is unequal, and would appear to be followed by an epibolic invagination. The outer layer of cells (epiblast) becomes covered with cilia, and the inner is transformed into a non-cellular (?) central yolk mass. At this stage the larva is hatched, and commences to lead a free existence. In the next stage observed by Metschnikoff, the mouth, oesophagus, stomach, and anus had become developed ; and two pairs of feet were present. In both of these feet Chaetopod-like setae were present, which in the hinder pair were simple fine bristles without a terminal hook. The papilliform portion of the foot is at first undeveloped. The feet become successively added, like Chaetopod segments, and the stomach does not become dendriform till the whole complement of feet (5 pairs) are present.
In the primitive covering of cilia, combined with a subsequent indication
1 Langerhans has recently made some important investigations on the nervous system of Sagitta, and identifies the ventral ganglion with the parieto-splanchnic ganglia of Molluscs, while he has found a pair of new ganglia, the development of which is unknown, which he calls the suboesophageal or pedal ganglia. The embryological facts do not appear to be in favour of these interpretations.
B. II. 24
of segments in the formation of the feet and setae, the larva of the Myzostomea shews an approximation to the Chaetopoda, and the group is probably to be regarded as an early Chactopod type specially modified in connection with its parasitic habits.
(379) L.Graff. Das Genus Myzostoma. Leipzig, 1877.
(380) E. Metschnikoff. "Zur Entwicklungsgeschichte d. Myzostomum." Zfit.f. wiss. Zool. y Vol. XVI. 1866.
(381) C. Semper. "Z. Anat. u. Entwick. d. Gat. Myzostomum." Ztit.f. wiss. Zool., Vol. ix. 1858.
A few observations of Ludwig on the winter eggs of Ichthydium larus shew that the segmentation is a total and apparently a regular one. It leads to the formation of a solid morula. The embryo has a ventral curvature, and the caudal forks are early formed as cuticular structures. By the time the embryo leaves the egg, it has almost reached the adult state. The ventral cilia arise some little time prior to the hatching.
(382) H. Ludwig. " Ueber die Ordnung Gastrotricha Mctschn" Zeit. f. wiss. Zool., Vol. xxvi. 1876.
CHAPTER XVI. NEMATELMINTHES AND ACANTHOCEPHALA
NEM ATELMINTHES '.
Nematoidea. Although the ova of various Nematodes have formed some of the earliest, as well as the most frequent objects of embryological observation, their development is still but very imperfectly known. Both viviparous and oviparous forms are common, and in the case of the oviparous forms the eggs are usually enveloped in a hard shell. The segmentation is total and nearly regular, though the two first segments are often unequal. The relation of the segmentation spheres to the germinal layers is however only satisfactorily established (through the researches of Butschli (No. 383)) in the case of Cucullanus elegans, a form parasitic in the Perch 2 .
The early development of this embryo takes place within the body of the parent, and the egg is enveloped in a delicate membrane. After the completion of the early stages of segmentation the embryo acquires the form of a thin flat plate composed of two layers of cells (fig. 166 A and B). The two layers of this plate give rise respectively to the epiblast and hypoblast, and at a certain stage the hypoblastic layer ceases to
1 The following classification of the Nematoda is employed in this chapter :
r Ascaridae. Strongylidae.
Trichinidse. II. Gordioidea.
I. Nematoidea. , Filarid8B . m . Chaetosomoidea.
Mermithidae. [_ Anguillulidse.
2 The ova of Anguillula aceti are stated by Hallez to undergo a similar development to those of Cucullanus.
grow, while the growth of the epiblastic layer continues. As a consequence of this the sides of the plate begin to fold over towards the side of the hypoblast (fig. 166 D.) This folding results in the formation of a remarkably constituted gastrula, which has the form of a hollow two-layered cylinder with an incompletely closed slit on one side (fig. 166 E, bl.p}. This slit has the value of a blastopore. It becomes closed by the coalescence of the two edges, a process which commences posteriorly,
A. B. C.
VARIOUS STAGES IN THE DEVELOPMENT OF CUCULLANUS ELEGANS.
Surface view of flattened embryo at an early stage in the segmentation. Side view of an embryo at a somewhat later stage, in optical section. Flattened embryo at the completion of segmentation.
D. Embryo at the commencement of the gastrula stage.
E. Embryo when the blastopore is reduced to a mere slit.
F. Vermiform embryo after the division of the alimentary tract into oesophageal and glandular divisions.
m. mouth; ep. epiblast; hy. hypoblast; me. mesoblast; a?, oesophagus; bl.p. blastopore.
and then gradually extends forwards. In front the blastopore never becomes completely closed, but remains as the permanent mouth. The embryo after these changes has a worm-like form, which becomes the more obvious as it grows in length and becomes curved (fig. 166 F).
The hypoblast of the embryo gives rise to the alimentary
canal, and soon becomes divided into an cesophageal section (fig. 1 66 F, ce) formed of granular cells, and a posterior division formed of clear cells. The mesoblast (fig. 166, me) takes its origin from certain special hypoblast cells around the mouth, and thence grows backwards towards the posterior end of the body.
The young Cucullanus becomes hatched while still in the generative ducts of its parent, and is distinguished by the presence of a remarkable thread-like tail. On the dorsal surface is a provisional boring apparatus in the form of a conical papilla. A firm cuticle enveloping the body is already present. In this condition it leaves its parent and host, and leads for a time a free existence in the water. Its metamorphosis is dealt with in another section.
The ova of the Oxyuridae parasitic in Insects are stated by Galeb (No. 386) to take the form of a blastosphere at the close of segmentation. An inner layer is then formed by delamination. What the inner layer gives rise to is not clear, since the whole alimentary canal is stated to be derived from two buds, which arise at opposite ends of the body, and grow inwards till they meet.
The generative organs. The study of the development of the generative organs of Nematodes has led to some interesting results. In the case of both sexes the generative organs originate (Schneider, No. 390) from a single cell. This cell elongates and its nuclei multiply. After assuming a somewhat columnar form, it divides into (i) a superficial investing layer, and (2) an axial portion.
In the female the superficial layer is only developed distinctly in the median part of the column. In the course of the further development the two ends of the column become the blind ends of the ovary, and the axial tissue they contain forms the germinal tissue of nucleated protoplasm. The superficial layer gives rise to the epithelium of the uterus and oviduct. The germinal tissue, which is originally continuous, is interrupted in the middle part (where the superficial layer gives rise to the uterus and oviduct), and is confined to the two blind extremities of the tube.
In the male the superficial layer, which gives rise to the epithelium of the vas deferens, is only formed at the hinder end of
the original column. In other respects the development takes place as in the female.
Gordioidea. The ovum of Gordius undergoes a regular segmentation. According to Villot (No. 391) it forms at the close of segmentation a morula, which becomes two-layered by delamination. The embryo is at first spherical, but soon becomes elongated.
By an invagination at the anterior extremity the head is formed. It consists of a basal portion, armed with three rings of stylets, and a conical proboscis, armed with three large stylets. When the larva becomes free the head becomes everted, though it remains retractile. By the time the embryo is hatched a complete alimentary tract is formed with an oral opening at the end of the proboscis, and a subterminal ventral anal opening. It is divided into an oesophagus and stomach, and a large gland opens into it at the base of the proboscis.
The body has a number of transverse folds, which give it a ringed appearance.
Metamorphosis and life history.
Nematoidea. Although a large number of Nematodes have a free existence and simple life history, yet the greater number of known genera are parasitic, and undergo a more or less complicated metamorphosis 1 . According to this metamorphosis they may be divided into two groups (which by no means closely correspond with the natural divisions), viz. those which have a single host, and those with two hosts. Each of these main divisions may be subdivided again into two.
In the first group with one host the simplest cases are those in which the adult sexual form of parasite lays its eggs in the alimentary tract of its host, and the eggs are thence transported to the exterior. The embryo still in the egg, if favoured by sufficient warmth and moisture, completes its development up to a certain point, and, if then swallowed by an individual of the species in which it is parasitic in the adult condition, it is denuded of its shell by the action of the gastric juice, and develops directly into the sexual form.
Leuckart has experimentally established this metamorphosis in the case of Trichocephalus affinis, Oxyurus ambigua, and Heterakis vermicularis. The Oxyuridae of Blatta and Hydrophilus have a similar life history
1 The following facts are mainly derived from Leuckart's exhaustive treatise (No. 388).
(Caleb, No. 386), and it is almost certain that the metamorphosis of the human parasites, Ascaris lumbricoides and Oxyurus vermicularis, is of this nature.
A slightly more complicated metamorphosis is common in the genera Ascaris and Strongylus. In these cases the egg-shell is thin, and the embryo becomes free externally, and enjoys for a shorter or longer period a free existence in water or moist earth. During this period it grows in size, and though not sexual usually closely resembles the adult form of the permanently free genus Rhabditis. In some cases the free larva becomes parasitic in a freshwater Mollusc, but without thereby undergoing any change. It eventually enters the alimentary tract of its proper host and there become sexual.
As examples of this form of development worked out by Leuckart may be mentioned Uochmius trigonocephalus, parasitic in the dog, and Ascaris acuminata, in the frog. The human parasite Dochmius duodenale undergoes the same metamorphosis as Dochmius trigonocephalus.
A remarkable modification of this type of metamorphosis is found in Ascaris (Rhabdonema) nigrovenosa, which in its most developed condition is parasitic in the lungs of the frog (Metschnikoff, Leuckart, No. 388). The embryos pass through their first developmental phases in the body of the parent. They have the typical Rhabditis form, and make their way after birth into the frog's rectum. From this they pass to the exterior, and then living either in moist earth, or the faeces of the frog, develop into a sexual form, but are very much smaller than in the adult condition. The sexes are distinct, and the males are distinguished from the females by their smaller size, shorter and rounded tails, and thinner bodies. The females have paired ovaries with a very small number of eggs, but the testis of the males is unpaired. Impregnation takes place in the usual way, and in summer time about four embryos are developed in each female, which soon burst their egg-capsules, and then move freely in the uterus. Their active movements soon burst the uterine walls, and they then come to lie freely in the body cavity. The remaining viscera of the mother are next reduced to a finely granular material, which serves for the nutrition of the young forms which continue to live in the maternal skin. The larvae eventually become free, and though in many respects different from the parent form which gave rise to them, have nevertheless the Rhabditis form. They live in water or slime, and sometimes become parasitic in water-snails ; in neither case however do they undergo important changes unless eventually swallowed by a frog. They then pass down the trachea into the lungs and there rapidly develop into the adult form. No separate males have been found in the lungs of the frog, but it has been shewn by Schneider (No. 390) that the so-called females are really hermaphrodites ; the same gland giving origin
to both spermatozoa and ova, the former being developed before the latter 1 . The remarkable feature of the above life history is the fact that in the stage corresponding with the free larval stage of the previous forms the larvae of this species become sexual, and give rise to a second free larval generation, which develops into the adult form on again becoming parasitic in the original host. It constitutes a somewhat exceptional case of heterogamy as defined in the introduction.
Amongst the Nematodes with but a single host a remarkable parasite in wheat has its place. This form, known as Anguillula scandens, inhabits in the adult condition the ears of wheat, in which it lays its eggs. After hatching, the larvae become encysted, but become free on the death of the plant. They now inhabit moist earth, but eventually make their way into the ears of the young wheat and become sexually mature.
The second group of parasitic Nematodes with two hosts may be divided into two groups, according to whether the larva has a free existence before passing into its first or intermediate host, or is taken into it while still in the egg. In the majority of cases the larval forms live in special connective tissue capsules, or sometimes free in the tissues of their intermediate hosts ; but the adults, as in the cases of other parasitic Nematodes, inhabit the alimentary tract.
The life history of Spiroptera obtusa may be cited as an example of a Nematode with two hosts in which the embryo is transported into its intermediate host while still within the egg. The adult of this form is parasitic in the mouse, and the ova pass out of the alimentary tract with the excreta, and may commonly be found in barns, etc. If one of the ova is now eaten by the meal-worm (larva of Tenebrio), it passes into the body cavity of this worm and undergoes further development. After about five weeks it becomes encapsuled between the ' fat bodies ' of the meal-worm. It then undergoes an ecdysis, and, if the meal-worm with its parasites is now eaten by the mouse, the parasites leave their capsule and develop into the sexual form.
As examples of life histories in which a free state intervenes before the intermediate host, Cucullanus elegans and Dracunculus may be selected. The adult Cucullanus elegans is parasitic in the alimentary tract of the Perch and other freshwater fishes. It is a viviparous form, and the young after birth pass out into the water. They next become parasitic in Cyclops, passing in through the mouth, so into the alimentary tract, and thence into the body cavity. They soon undergo an ecdysis, in the course of which the oesophagus becomes divided into a muscular pharynx and true glandular
1 Leuckart does not appear to be satisfied as to the hermaphroditism of these forms ; and holds that it is quite possible that the ova may develop parthenogenetically.
oesophagus. They then grow rapidly in length, and at a second ecdysis acquire a peculiar beaker-like mouth cavity approaching that of the adult. They do not become encapsuled. No further development of the worm takes place so long as it remains in the Cyclops, but, if the Cyclops is now swallowed by a Perch, the worm undergoes a further ecdysis, and rapidly attains to sexual maturity.
The observations of Fedschenko on Dracunculus medinensis 1 , which is parasitic in the subcutaneous connective tissue in Man, would seem to shew that it undergoes a metamorphosis very similar to that of Cucullanus. There is moreover a striking resemblance between the larvae of the two forms. The larvae of Dracunculus become transported into water, and then make their way into the body cavity of a Cyclops by boring through the soft skin between the segments on the ventral surface of the body. In the body cavity the larvae undergo an ecdysis and further development. But on reaching a certain stage of development, though they remain a long time in the Cyclops, they grow no further. The remaining history is unknown, but probably the next host is man, in which the larva comes to maturity. In the adult condition only females of Dracunculus are known, and it has been suggested by various writers that the apparent females are in reality hermaphrodites, like Ascaris nigrovenosa, in which the male organs come to maturity before the female.
Another very remarkable human parasite belonging to the same group as Dracunculus is the form known as Filaria sanguinis hominis, or Filaria Bancrofti 2 .
The sexual form is parasitic in warm climates in the human tissues, and produces multitudes of larvae which pass into the blood, and are sometimes voided with the urine. The larvae in the blood do not undergo a further development, and unless transported to an intermediate host die before very long. Some, though as yet hardly sufficient, evidence has been brought forward to shew that if the blood of an infected patient is sucked by a mosquito the larvae develop further in the alimentary tract of the mosquito, pass through a more or less quiescent stage, and eventually grow considerably in size, and on the death of the mosquito pass into the water. From the water they are probably transported directly or indirectly into the human intestines, and then bore their way into the tissues in which they are parasitic, and become sexually mature.
The well-known Trichina spiralis has a life history unlike that of other known Nematodes, though there can be little doubt that this form should be classified in respect to its life history with the last- described forms. The peculiarity of the life history of Trichina is that the embryos set free in the alimentary canal pass through the walls into the muscular tissues and there encyst ; but do not in a general way pass out from the alimentary
1 Vide Leuckart, D. men. Par., Vol. II. p. 704.
2 Vide D. P. Manson, " On the development of Filaria sanguinis hominis." Journal of the Linnean Society, Vol. xiv. No. 75.
canal of one host and thence into a fresh host to encyst. It occasionally however happens that this migration does take place, and the life history of Trichina spiralis then becomes almost identical with that of some of the forms of the third type. Trichina is parasitic in man, and in swine, and also in the rat, mouse, cat, fox and other forms which feed upon them. Artificially it can be introduced into various herbivorous forms (rabbit, guinea-pig, horse) and even birds.
The sexual form inhabits the alimentary canal. The female is viviparous, and produces myriads of embryos, which pass into the alimentary canal of their host, through the walls of which they make their way, and travelling along lines of connective tissue pass into the muscles. Here the embryos, which are born in a very imperfect condition, rapidly develop, and eventually assume a quiescent condition in a space inclosed by sarcolemma. Within the sarcolemma a firm capsule is developed for each larva, which after some months becomes calcified ; and after the atrophy of the sarcolemma a connective tissue layer is formed around it. Within its capsule the larva can live for many years, even ten or more, without undergoing further development, but if at last the infected flesh is eaten by a suitable form, e.g. the infected flesh of the pig by man, the quiescent state of the larva is brought to a close, and sexual maturity is attained in the alimentary tract of the new host.
Gordioidea. The free larva of Gordius already described usually penetrates into the larva of Chironomus where it becomes encysted. On the Chironomus being eaten by some fish (Villot, No. 39) (Phoxinus laevis or Cobitis barbatula), it penetrates into the wall of the intestine of its second host, becomes again encysted and remains quiescent for some time. Eventually in the spring it leaves its capsule, and enters the intestine, and passes to the exterior with the faeces. It then undergoes a gradual metamorphosis, in the course of which it loses its ringed structure and cephalic armature, grows in length, acquires its ventral cord, and on the development of the generative organs loses the greater part of its alimentary tract.
Young examples of Gordius have often been found in various terrestrial carnivorous Insecta, but the meaning of this fact is not yet clear.
(383) O. Biitschli. "Entwicklungsgeschichte d. Cucullanus elegans." Zdt.j. wiss. Zool., B. xxvi. 1876.
(384) T. S. Cobbold. Entozoa. Groombridge and Son, 1864.
(385) T. S. Cobbold. Parasites; A Treatise on the Entozoa of Man mn/ Animals. Churchill, 1879.
(386) O. Galeb. "Organisation et developpement des Oxyurides," &c. Archives de Zool. expcr. et getter. , Vol. vn. 1878.
(387) R. Leu ck art. Untcrsufkutigcn itb. Trichina spiralis. 2nd ed. Leip/ig, 1866.
(388) R. Leuckart. Die tnenschlichcn Parasitcn, Bd. II. 1876.
(389) H. A. Pagenstecher. Die Trichinen nach Versitchen dargestellt. Leipzig, 1865.
(390) A.Schneider. Monographic d. Nemaioden. Berlin, 1866.
(391) A. Villot. "Monographic des Dragoneaux" (Gordioidea). Archives de Zool. exper. et gener., Vol. ill. 1874.
The Acanthocephala appear to be always viviparous. At the time of impregnation the ovum is a naked cell, and undergoes in this condition the earlier phases of segmentation.
The segmentation is unequal (Leuckart, No. 393), but whether there is an epibolic gastrula has not clearly been made out.
Before segmentation is completed there are formed round the ovum thick protecting membranes, which are usually three in number, the middle one being the strongest. After segmentation the central cells of the ovum fuse together to give rise to a granular mass, while the peripheral cells at a slightly later period form a more transparent syncytium. At the anterior end of the embryo there appears a superficial cuticle bearing in front a ring of hooks.
The embryo is now carried out with the excreta from the intestine of the vertebrate host in which its parent lives. It is then swallowed by some invertebrate host 1 .
In the intestine of the invertebrate host the larva is freed from its membranes, and is found to have a somewhat elongated conical form, terminating anteriorly in an obliquely placed disc, turned slightly towards the ventral surface and armed with hooks. Between this disc and the granular mass, already described as formed from the central cells of the embryo, is a rather conspicuous solid body. Leuckart supposes that this body may represent a rudimentary functionless pharynx, while the granular mass in his opinion is an equally rudimentary and functionless intestine. The body wall is formed of a semifluid internal layer surrounding the rudimentary intestine, if such it be, and of a firmer outer wall immediately within the cuticle. The adult Echinorhyncus is formed by a remarkable process of development within the body of the larva, and the skin is the only part of the larva which is carried over to the adult.
In Echinorhyncus proteus the larva remains mobile during the formation of the adult, but in other forms the metamorphosis takes place during a quiescent condition of the larva.
The organs of the adult are differentiated from a mass of cells which appears to be a product of the central embryonic granular mass, and is
1 Echin. proteus, which is parasitic in the adult state in many freshwater fish, passes through its larval condition in the body cavity of Gammarus pulex. Ech. angustatus, parasitic in the Perch, is found in the larval condition in the body cavity of Asellus aquaticus. Ech. gigas, parasitic in swine, is stated by Schneider (No. 394) to pass through its larval stages in maggots.
called by Leuckart the embryonic nucleus. The embryonic nucleus becomes divided into four linearly arranged groups of cells, of which the hindermost but one is the largest, and very early differentiates itself into (i) a peripheral layer, and (2) a central mass formed of two distinct bodies. The peripheral layer of this segment grows forwards and backwards, and embraces the other segments, with the exception of the front end of the first one which is left uncovered. The envelope so formed gives rise to the splanchnic and somatic mesoblast of the adult worm. Of the four groups of cells within it the anterior gives rise to the proboscis, the next to the nerve ganglion, the third, formed of two bodies, to the paired generatives, and the fourth to the generative ducts. The whole of the above complex rapidly elongates, and as it does so the enveloping membrane becomes split into two layers ; of which the outer forms the muscular wall of the body (somatic mesoblast), and the inner the muscular sheath of the proboscis and the so-called generative ligament enveloping the generative organs. The inner layer may be called the splanchnic mesoblast in spite of the absence of an intestine. The cavity between the two mesoblastic layers forms the body cavity.
The various parts of the adult continue to differentiate themselves as the whole increases in size. The generative masses very early shew traces of becoming differentiated into testes or ovaries. In the male the two generative masses remain spherical, but in the female become elongated : the rudiment of the generative ducts becomes divided into three sections in both sexes. The most remarkable changes are, however, those undergone by the rudiment of the proboscis.
In its interior there is formed a cavity, but the wall bounding the front end of the cavity soon disappears. By the time that this has taken place the body of the adult completely fills up the larval skin, to which it very soon attaches itself. The hollow rudiment of the proboscis then becomes everted, and forms a papilla at the end of the body, immediately adjoining the larval skin. This papilla, with the larval skin covering it, constitutes the permanent proboscis. The original larval cuticle is either now or at an earlier period thrown off and a fresh cuticle developed. The hooks of the proboscis are formed from cells of the above papilla, which grow through the larval skin as conical prominences, on the apex of which a chitinous hook is modelled. The remainder of the larval skin forms the skin of the adult, and at a later period develops in its deeper layer the peculiar plexus of vessels so characteristic of the Acanthocephala. The anterior oval appendages of the adult cutis, known as the lemnisci, are outgrowths from the larval skin.
The Echinorhyncus has with the completion of these changes practically acquired its adult structure ; but in the female the ovaries undergo at this period remarkable changes, in that they break up into a number of spherical masses, which lie in the lumen of the generative ligaments, and also make their way into the body cavity.
The young Echinorhyncus requires to be transported to its permanent host, which feeds on its larval host, before attaining to sexual maturity.
(392) R. Greeff. " Untersuchungen ii. d. Bau u. Entwicklung des Echin. miliarius." Archiv f. Naturgesch. 1864.
(393) R. Leuckart. Die menschlichen Parasiten. Vol. n. p. 80 1 et seq. 1876.
(394) An. Schneider. " Ueb. d. Bau d. Acanthocephalen." Archiv f. Anat. u, Phys. 1868.
(395) G. R. Wagener. Beitrdge z. Entwicklungsgeschichte d. Eingeweidewiirmer. Haarlem, 1865.
PROTOTRACH EAT A. THE remarkable researches of Moseley (No. 396) on Peripatus
FIG. 167. ADULT EXAMPLE OF PERIPATUS CAPENSIS, natural size. (From Moseley.)
capensis have brought clearly to light the affinities of this form with the tracheate Arthropoda ; and its numerous primitive
FIG. 168. Two STAGES IN THE DEVELOPMENT OF PERIPATUS CAPENSIS. (After Moseley.)
A. Youngest stage hitherto observed before the appearance of the legs.
B. Later stage after the legs and antennae have become developed. Both figures represent the larva as it appears within the egg.
i and i. First and second post-oral appendages.
characters, such as the generally distributed tracheal apertures, the imperfectly segmented limbs, the diverging ventral nerve
cords with imperfectly marked ganglia, and the nephridia (segmental organs 1 ), would render its embryology of peculiar interest. Unfortunately Moseley was unable, from want of material, to make so complete a study of its development as of its anatomy. The youngest embryo observed was in part distinctly segmented, and coiled up within the egg (fig. 168 A). The procephalic lobes resemble those of the Arthropoda generally, and are unlike the prae-oral lobe of Chaetopods or Discophora. They are not marked off by a transverse constriction from the succeeding segments. The three embryonic layers are differentiated, and the interior is filled with a brownish mass the remnant of the yolk which is probably enclosed in a distinct intestinal wall, and is lobed in correspondence with the segmentation of the body. The mouth invagination is not present, and but two pairs of slight prominences mark the rudiments of the two anterior post-oral appendages.
The single pair of antennae is formed in the next stage, and is followed by the remaining post-oral appendages, which arise in succession from before backwards somewhat later than the segments to which they appertain.
The posterior part of the embryo becomes uncoiled, and the whole embryo bent double in the egg (fig. 168 B).
The mouth appears as a slit-like opening between and below the procephalic lobes. On each side and somewhat behind it there grows out an appendage the first post-oral pair (fig. 169, i) while in front and behind it are formed the upper and lower lips. These two appendages next turn inwards towards the mouth, and their
FIG. 169. EMBRYO OF PERIPATUS CAPENSIS. Slightly older than A in fig. 168; unrolled. (After Moseley.)
a. antennae ; o. mouth ; i. intestine ; c. procephalic lobe, i, 2, 3, etc., postoral appendages.
1 F. M. Balfour, "On certain points in the Anatomy of Peripatus capensis." Quart. Journ. of Micros. Science, Vol. xix. 1879.
bases become gradually closed over by two processes of the procephalic region (fig. 170, m) The whole of these structures assist in forming a kind of secondary mouth cavity, which is at a later period further completed by the processes of the procephalic region meeting above the mouth, covering over the labrum, and growing backwards to near the origin of the second pair of post-oral appendages.
The antennae early become jointed, and fresh joints continue to be added throughout embryonic life ; in the adult there are present fully thirty joints. It appears to me probable (though Mr Moseley takes the contrary view) from the late development of the paired processes of the procephalic lobes, which give rise to the circular lip of the adult, that they are not true appendages. The next pair therefore to the antennae is the first post-oral pair. It is the only pair connected with the mouth. At their extremities there is formed a pair of claws similar to those of the ambulatory
legs (fig. 171). The next FIG. 171. HEAD OF AN EMBRYO PERIPA, . . r TUS. (From Moseley.)
and largest pair of appen- The figure shews the jaws (mamlil)lcs)> and
dagCS in the embryo are close to them epiblastic involutions, which
FIG. 170. VENTRAL VIEW OF THE HEAD OF AN EMBRYO OF PERIPATUS CAPENSIS AT A LATE STAGE OF DEVELOPMENT.
/. thickening of epiblast of procephalic lobe to form supra-oesophageal ganglion ; ///. process from procephalic lobe growing over the first post-oral appendage ; o. mouth; e. eye; i and 2, first and second pair of post-oral appendages.
the oral papillae. They
grow into the supra-oesophageal ganglia. The antennae, oral cavity, and oral papilhe are also
are chiefly remarkable for shewn.
containing the ducts of the slime glands which open at their bases. They are without claws. The succeeding appendages become eventually imperfectly five-jointed ; two claws are
formed as cuticular investments of papillae in pockets of the skin at the ends of their terminal joints.
I have been able to make a few observations on the internal structure of the embryos from specimens supplied to me by Moseley. These are so far confined to a few stages, one slightly earlier, the others slightly later, than the embryo represented in fig. 168 B. The epiblast is formed of a layer of columnar cells, two deep on the ventral surface, except along the median line where there is a well-marked groove and the epiblast is much thinner (fig. 172).
The ventral cords of the trunk are formed as two independent epiblastic thickenings. In my earlier stage these are barely separated from the epiblast, but in the later ones are quite independent (fig. 172, v.n), and partly surrounded by mesoblast.
The supra-cesophageal ganglia are formed as thickenings of the epiblast of the ventral side of the procephalic lobes in front of the stomodaeum. They are shewn at / in fig. 170. The thickenings of the two sides are at first independent. At a somewhat later period an invagination of the epiblast grows into each of these lobes. The openings of these invaginations extend from the oral cavity forwards; and they are shewn in fig. 171 l . Their openings become closed, and the walls of the invaginations constitute a large part of the embryonic supra-cesophageal ganglia.
Similar epiblastic invaginations assist in forming the supra-cesophageal ganglia of other Tracheata. They are described in the sequel for Insects, Spiders and Scorpions. The position of the supracesophageal ganglia on the ventral side of the procephalic lobes is the same as that in other Tracheata.
The mesoblast is formed, in the earliest of my embryos, of scattered cells in the fairly wide space between the mesenteron and the epiblast. There are two distinct bands of mesoblast on the outer sides of the nervous cords. In the later stage the mesoblast is divided into distinct somatic and splanchnic layers, both very thin ; but the two layers are connected by transverse strands (fig. 172). There
FIG. 172. SECTION THROUGH THE TRUNK OF AN EMBRYO OF PERIPATUS. The embryo from which the section is taken was somewhat younger than fig. 171.
sp.m. splanchnic mesoblast.
s.m. somatic mesoblast.
me. median section of body cavity.
k. lateral section of body cavity.
v.n. ventral nerve cord.
1 This figure is taken from Moseley. The epiblastic invaginations are represented in it very accurately, and though not mentioned in the text of the paper, Moseley informs me that he has long been aware of the homology of these folds with those in various other Tracheata.
are two special longitudinal septa dividing the body cavity into three compartments, a median (me), containing the mesenteron, and two lateral (Ic) containing the nerve cords. This division of the body cavity persists, as I have elsewhere shewn, in the adult. A similar division is found in some Chaetopoda, e.g. Polygordius.
I failed to make out that the mesoblast was divided into somites, and feel fairly confident that it is not so in the stages I have investigated.
There is a section of the body cavity in the limbs as in embryo Myriapods, Spiders, etc.
In the procephalic lobe there is a well-developed section of the body cavity, which lies dorsal to and in front of the rudiment of the supracesophageal ganglia.
The alimentary tract is formed of a mesenteron (fig. 172), a stomodaeum, and proctodaeum. The wall of the mesenteron is formed, in the stages investigated by me, of a single layer of cells with yolk particles, and encloses a lumen free from yolk. The forward extension of the mesenteron is remarkable.
The stomodaeum in the earlier stage is a simple pit, which meets but does not open into the mesenteron. In the later stage the external opening of the pit is complicated by the structures already described. The proctodaeum is a moderately deep pit near the hinder end of the body.
The existence of a tracheal system 1 is in itself almost sufficient to demonstrate the affinities of Peripatus with the Tracheata, in spite of the presence of nephridia. The embryological characters of the procephalic lobes, of the limbs and claws, place however this conclusion beyond the reach of scepticism. If the reader will compare the figure of Peripatus with that of an embryo Scorpion (fig. 196 A) or Spider (fig. 200 C) or better still with Metschnikoffs figure of Geophilus (No. 399) PI. xxi. fig. u,he will be satisfied on this point.
The homologies of the anterior appendages are not very easy to determine ; but since there does not appear to me to be sufficient evidence to shew that any of the anterior appendages have become aborted, the first post-oral appendages embedded in the lips may provisionally be regarded as equivalent to the mandibles, and the oral papillae to the first pair of maxillae, etc. Moseley is somewhat doubtful about the homologies of the appendages, and hesitates between considering the oral papillae as equivalent to the second pair of maxillae (on account of their containing the openings of the mucous glands, which he compares with the spinning glands of caterpillars), or to the poison claws (fourth
1 The specimens shewing tracheae which Moseley has placed in my hands are quite sufficient to leave no doubt whatever in my mind as to the general accuracy of his description of the tracheal system.
post-oral appendages) of the Chilopoda (on account of the poison-glands which he thinks may be homologous with the mucous glands).
The arguments for either of these views do not appear to me conclusive. There are glands opening into various anterior appendages in the Tracheata, such as the poison glands in the Chelicerae (mandibles) of Spiders, and there is some evidence in Insects for the existence of a gland belonging to the first pair of maxillae, which might be compared with the mucous gland of Peripatus. For reasons already stated I do not regard the processes of the cephalic lobes, which form the lips, as a pair of true appendages.
(396) H. N. Moseley. "On the Structure and Development of Peripatus capensis." Phil. Trans. Vol. 164, 1874.
MYRIAPODA 1 .
Chilognatha. The first stages in the development of the Chilognatha have been investigated by Metschnikoffand Stecker, but their accounts are so contradictory as hardly to admit of reconciliation.
According to Metschnikoff, by whom the following four species have been investigated, viz., Strongylosoma Guerinii, Polydesmus complanatus, Polyxenus lagurus, and Julus Moneletei, the segmentation is at first regular and complete, but, when the segments are still fairly large, the regular segmentation is supplemented by the appearance of a number of small cells at various points on the surface, which in time give rise to a continuous blastoderm.
The blastoderm becomes thickened on the ventral surface, and so forms a ventral plate 2 .
1 The classification of the Myriapoda employed in the present section is
I. Chilognatha. (Millipedes.) II. Chilopoda. (Centipedes.)
2 Stecker's (No. 400) observations were made on the eggs of Julus fasciatus, Julus fcetidus, Craspedosoma marmoratum, Polydesmus complanatus, and Strongylosoma pallipes, and though carried on by means of sections, still leave some points very obscure, and do not appear to me deserving of much confidence. The two species of Julus and Craspedosoma undergo, according to Stecker, a nearly identical development. The egg before segmentation is constituted of two substances, a central protoplasmic, and a peripheral deutoplastic. It first divides into two equal segments, and coincidentally with their formation part of the central protoplasm travels to the
FIG. 173. THREE STAGES IN THE DEVELOPMENT OF STRONGYLOSOMA GUERINII. (After Metschnikoff.)
A. Embryo on eleventh day with commencing ventral flexure (*).
B. Embryo with three pairs of post-oral appendages.
C. Embryo with five pairs of post-oral appendages.
gs. ventral plate; at. antenme; 15 post-oral appendages; x. point of flexure of the ventral plate.
surface as two clear fluid segments. The ovum is thus composed of two yolk segments to two protoplasmic segments. The two former next divide into four, with the production of two fresh protoplasmic segments. The four protoplasmic segments now constitute the upper or animal pole of the egg, and occupy the position of the future ventral plate. The yolk segments form the lower pole, which is however dorsal in relation to the future animal. The protoplasmic segments increase in number by a regular division, and arrange themselves in three rows, of which the two outermost rapidly grow over the yolk segments. A large segmentation cavity is stated to be present in the interior of the ovum.
It would appear from Stecker's description that the yolk segments (hypoblast) next become regularly invaginated, so as to enclose a gastric cavity, opening externally by a blastopore; but it is difficult to believe that a typical gastrula, such as that represented by Sleeker, really comes into the cycle of development of the Chilognatha.
The mesoblast is stated to be derived mainly from the epiblast. This layer in the region of the future ventral plate becomes reduced to two rows of cells, and the inner of these by the division of its constituent elements gives rise to the mesoblast. The development of Polydesmus and Strongylosoma is not very different from that of Julus. The protoplasm at the upper pole occupies from the first a superficial position. Segmentation commences at the lower pole, where the food yolk is mainly present ! The gastrula is stated to be similar to that of Julus, The mesoblast is formed in Polydesmus as a layer of cells split off from the epiblast, but in Strongylosoma as an outgrowth from the lips of the blastopore. Stecker, in spite of the statements in his paper as to the origin of the mesoblast from the epiblast, sums up at the end to the effect that both the primary layers have a share in the formation of the mesoblast, which originates by a process of endogenous cell-division !
It may be noted that the closure of the blastopore takes place, according to Stecker, on the dorsal side of the embryo.
The most important sources of information for the general embryology of the Chilognatha are the papers of Newport (No. 397) and Metschnikoff (No. 398). The development of Strongylosoma may be taken as fairly typical for the group ; and the subsequent statements, unless the reverse is stated, apply to the species of Strongylosoma investigated by Metschnikoff.
After the segmentation and formation of the layers the first observable structure is a transverse furrow in the thickening of the epiblast on the ventral surface of the embryo. This furrow rapidly deepens, and gives rise to a ventral flexure of the embryo (fig. 173 A, x\ which is much later in making its appearance in Julus than in Strongylosoma and Polyxenus. A pair of appendages, which become the antennae, makes its appearance shortly after the formation of the transverse furrow, and there soon follow in order the next three pairs of appendages. All these parts are formed in the infolded portion of the ventral thickening of the blastoderm (fig. 173 B). The ventral thickening has in the meantime become marked by a longitudinal furrow, but whether this is connected with the formation of the nervous system, or is equivalent to the mesoblastic furrow in Insects, and connected with the formation of the mesoblast, has not been made out. Shortly after the appearance of the three pairs of appendages behind the antennae two further pairs become added, and at the same time oral and anal invaginations become formed '(fig- 173 Q. In front of the oral opening an unpaired upper lip is developed. The prse-oral part of the ventral plate develops into the bilobed procephalic lobes, the epiblast of which is mainly employed in the formation of the supra-cesophageal ganglia. The next important change which takes place is the segmentation of the body of the embryo (fig. 174 A), the most essential feature in which is the division of the mesoblast into somites. Segments are formed in order from before backwards, and soon extend to the region behind the appendages. On the appearance of segmentation the appendages commence to assume their permanent form. The two anterior pairs of post-oral appendages become jaws ; and the part of the embryo which carries them and the antennae is marked off from the trunk as the head. The three following pairs of appendages grow in length and assume a form suited for locomotion. Behind
the three existing pairs of limbs there are developed three fresh pairs, of whicJi tJie two anterior belong to a single primitive segment. While the above changes take place in the appendages the embryo undergoes an ecdysis, which gives rise to a cuticular membrane within the single egg-membrane (chorion, Metschnikoff\ On this cuticle a tooth-like process is developed, the function of which is to assist in the hatching of the embryo (fig. 174 A).
In Polyxenus a cuticular membrane is present as in Strongylosoma, but it is not provided with a tooth-like process. In the same form amoeboid cells separate themselves from the blastoderm at an early period. These cells have been compared to the embryonic envelopes of Insects described below.
In Julus two cuticular membranes are present at the time of hatching : the inner one is very strongly developed and encloses the embryo after hatching. After leaving the chorion the embryo Julus remains connected with it by a structureless membrane which is probably the outer of the two cuticular membranes.
At the time when the embryo of Strongylosoma is hatched (fig. 174 B) nine post-cephalic segments appear to be present.
FlG. 174. TWO STAGES IN THE DEVELOPMENT OF STRONGYLOSOMA GUEKINll.
A. A seventeen days' embryo, already segmented.
B. A just-hatched larva.
Of these segments the second is apparently (from MetschnikofT's figure, 174 B) without a pair of appendages; the third and
fourth are each provided with a single functional pair of limbs ; the fifth segment is provided with two pairs of rudimentary limbs, which are involuted in a single sack and not visible without preparation, and therefore not shewn in the figure. The sixth segment is provided with but a single pair of" appendages, though a second pair is subsequently developed on it 1 .
Julus, at the time it leaves the chorion, is imperfectly segmented, but is provided with antennas, mandibles, and maxillae, and seven pairs of limbs, of which the first three are much more developed than the remainder. Segmentation soon makes its appearance, and the head becomes distinct from the trunk, and on each of the three anterior trunk segments a single pair of limbs is very conspicuous (Metschnikoff) 2 . Each of the succeeding segments bears eventually two pairs of appendages. At the time when the inner embryonic cuticle is cast off, the larva appears to be hexapodous, like the young Strongylosoma, but there are in reality four pairs of rudimentary appendages behind the three functional pairs. The latter only appear on the surface after the first post-embryonic ecdysis. Pauropus (Lubbock) is hexapodous in a young stage. At the next moult two pairs of appendages are added, and subsequently one pair at each moult.
There appear to be eight post-oral segments in Julus at the time of hatching. According to Newport fresh segments are added in post-embryonic life by successive budding from a blastema between the penultimate segment and that in front of it. They arise in batches of six at the successive ecdyses, till the full number is completed. A functional, though not a real hexapodous condition, appears to be characteristic of Chilognatha generally at the time of hatching.
The most interesting anatomical feature of the Chilognatha is the double character of their segments, the feet (except the first three or four, or more), the circulatory, the respiratory, and the nervous systems shewing this peculiarity. Newport's and
1 Though the superficially hexapodous larva of Strongylosoma and other Chilognatha has a striking resemblance to some larval Insects, no real comparison is possible between them, even on the assumption that the three functional appendages of both are homologous, because Embryology clearly proves that the hexapodous Insect type has originated from an ancestor with numerous appendages by the atrophy of those appendages, and not from an hexapodous larval form prior to the development of the full number of adult appendages.
2 Newport states however that a pair of limbs is present on the first, second, and fourth post-oral segments, but that the third segment is apodous ; and this is undoubtedly the case in the adult.
Metschnikoff's observations have not thrown as much light on the nature of the double segments as might have been hoped, but it appears probable that they have not originated from a fusion of two primitively distinct segments, but from a later imperfect division of each of the primitive segments into two, and the supply to each of the divisions of a primitive segment of a complete set of organs.
Chilopoda. Up to the present time the development of only one type of Chilopoda, viz. that of Geophilus, has been worked out. Most forms lay their eggs, but Scolopendra is viviparous.
a u . i
FlG. 175. TWO STAGES IN THE DEVELOPMENT OF GEOPHILUS.
A. Side-view of embryo at the stage when the segments are beginning to be formed.
B. Later stage after the appendages have become established.
at. antenna.-; an.t. proctodseum.
The segmentation appears to resemble that in the Chilognatha, and at its close there is present a blastoderm surrounding a central mass of yolk cells. A ventral thickening of the blastoderm is soon formed. It becomes divided into numerous segments, which continue to be formed successively from the posterior unsegmented part. The antennae are the first appendages to appear, and are well developed when eighteen segments have become visible (fig. 175 A). The post-oral appendages are formed slightly later, and in order from before backwards. As the embryo grows in length, and fresh segments continue to be formed, the posterior part of it becomes bent over so as to face the ventral surface of the anterior, and it acquires an
appearance something like that of many embryo Crustaceans (fig. 175 B). Between forty and fifty segments are formed while the embryo is still in the egg. The appendages long remain unjointed. The fourth post-oral appendage, which becomes the poison-claw, is early marked out by its greater size : on the third post-oral there is formed a temporary spine to open the egg membrane.
It does not appear, from Metschnikoff's figures of Geophilus, that any of the anterior segments are without appendages, and it is very probable that Newport is mistaken in supposing that the embryo has a segment without appendages behind that with the poison claws, which coalesces with the segment of the latter. It also appears to me rather doubtful whether the third pair of post-oral appendages, i.e. those in front of the poison-claws, can fairly be considered as forming part of the basilar plate. The basilar plate is really the segment of the poison-claws, and may fuse more or less completely with the segment in front and behind it, and the latter is sometimes without a pair of appendages (Lithobius, Scutigera).
Geophilus, at the time of birth, has a rounded form like that of the Chilognatha.
The young of Lithobius is born with only six pairs of limbs.
General observation on the homologies of the appendages of Myriapoda.
The chief difficulty in this connection is the homology of the third pair of post-oral appendages.
In adult Chilognatha there is present behind the mandibles a four-lobed plate, which is usually regarded as representing two pairs of appendages, viz. the first and second pairs of maxillae of Insects. Metschnikoff's observations seem however to shew that this plate represents but a single pair of appendages, which clearly corresponds with the first pair of maxillae in Insects. The pair of appendages behind this plate is ambulatory, but turned towards the head ; it is in the embryo the foremost of the three functional pairs of legs with which the larva is born. Is it equivalent to the second pair of maxillae of Insects or to the first pair of limbs of Insects? In favour of the former view is the fact (i) that in embryo Insects the second pair of maxillae sometimes resembles the limbs rather than the jaws, so that it might be supposed that in Chilognatha a primitive ambulatory condition of the third pair of appendages has been retained ; (2) that the disappearance of a pair of appendages would have to be postulated if the second alternative is adopted, and that if Insects are descended from forms related to the Myriapods it is surprising to find a pair of appendages always present in the former, absent in the latter.
The arguments which can be urged for the opposite view do not appear to me to have much weight, so that the homology of the appendages in question with the second pair of maxillae may be provisionally assumed.
The third pair of post-oral appendages of the Chilopoda may probably also be assumed to be equivalent to the second pair of maxillae, though they are limb-like and not connected with the head. The subjoined table shews the probable homologies of the appendages.
CHILOGNATHA(Strongylo so ma at time of birth).
CHILOPODA (Scolopendra adult).
ist Post-oral segment.
2nd ,, ,,
Maxillae i. (Four-lobed plate in adult, but a simple pair of appendages in embryo).
Maxillie i. (Palp and bilobed median process).
3rd (probably equivalent to segment bearing 2nd pair of maxillae in Insects).
ist pair of ambulatory limbs.
Limb-like appendages with basal parts in contact.
4th ,, ,,
2nd pair of ambulatory limbs.
ist pair of ambulatory limbs.
4th and sth (rudimentary. )
8th ,, ,,
6th (the 7th pair is developed in this segment later).
,, (last segment in embryo).
The germinal layers and formation of organs.
The development of the organs of the Myriapoda, and the origin of the germinal layers, are very imperfectly known : Myriapoda appear however to be closely similar to Insects in this part of their development, and the general question of the layers will be treated more fully in connection with that group.
The greater part of the blastoderm gives rise to the epiblast, which furnishes the skin, nervous system, tracheal system, and the stomodacum and proctodaeum.
The mesoblast arises in connection with the ventral thickening of the blastoderm, but the details of its formation are not known. Metschnikoff describes a longitudinal furrow which appears very early in Strongylosoma, which is perhaps equivalent to the mesoblastic furrows of Insects, and so connected with the formation of the mesoblast.
The mesoblast is divided up into a series of protovertebra-like bodies the mesoblastic somites the cavities of which become the body cavity and the walls the muscles and probably the heart. They are (Metschnikoff) prolonged into the legs, though the prolongations become subsequently segmented off from the main masses. The splanchnic mesoblast is, according to Metschnikoff, formed independently of the somites, but this point requires further observation.
The origin of the hypoblast remains uncertain, but it appears probable that it originates, in a large measure at least, from the yolk segments. In the Chilognatha the mesenteron is formed in the interior of the yolk segments, so that those yolk segments which are not employed in the formation of the alimentary canal lie freely in the body cavity. In the relation of the yolk segments to the alimentary canal the Chilopoda present a strong contrast to the Chilognatha, in that the greater part of the yolk lies within their mesenteron. The mesenteron is at first a closed sack, but is eventually placed in communication with the stomodaeum and the proctodasum. The Malpighian bodies arise as outgrowths from the blind extremity of the latter.
(397) G. N e wp or t. " On the Organs of Reproduction and Development of the Myriapoda." Philosophical Transactions, 1841.
(398) E. Metschnikoff. ' ' Embryologie der doppeltflissigen Myriapoden (Chilognatha)." Zeit.f. wiss. Zool., Vol. xxiv. 1874.
(399) ' ' Embryologisches iiber Geophilus." Zeit. f. wiss. ZooL y Vol. xxv.
1875 (400) Anton Stecker. "Die Anlage d. Keimblatter bei den Diplopoden." Archivf. mik. Anatomie, Bd. xiv. 1877.
INSECTA 1 .
The formation of the embryonic layers in Insects has not been followed out in detail in a large number of types ; but, as
1 The following classification of the Insecta is employed in this chapter, ((i) Collembola.
I. Aptera. | (a) Thysanura .
!(i) Orthoptera genuina (Blatta, Locusta, etc.). (2) pseudoneuroptera (Termes, Ephemera,
!(i) Hemiptera heteroptera (Cimex, Notonecta, etc.). (2) ,, homoptera (Aphis, Cicada, etc.).
(3) ,, parasita (Pediculus, etc.).
in so many other instances, some of the most complete histories we have are due to Kowalevsky (No. 416). The development
FiG. 176. FOUR EMBRYOS OF llYDROPHlLUS P1CEUS VIEWED FROM THE
VENTRAL SURFACE. (After Kowalevsky.) The upper end is the anterior, gg. germinal groove; am. amnion.
of Hydrophilus has been worked out by him more fully than that of any other form, and will serve as a type for comparison with other forms.
The segmentation has not been studied, but no doubt belongs to the centrolecithal type (vide pp. no 120). At its close there is an uniform layer of cells enclosing a central mass of yolk. These cells, in the earliest observed stage, were flat on the dorsal, but columnar on part of the ventral surface of the egg, where they form a thickening which will be called the ventral plate. At the posterior part of the ventral plate two folds, with a furrow between them, make their appearance. They form a structure which may be spoken of as the germinal groove (fig.
!(i) Diptera genuina (Musca, Tipula, etc.). (2) aphaniptera (Pulex, etc.). (3) ,, pupipara (Braula, etc.).
v .. ( (i) Neuroptera planipennia (Myrniclcon, etc.) TOptera. j (a) ^ trichoptera (Phryganea, etc.).
VI. Coleoptera. VII. Lepidoptera.
(i) Hymenoptera aculeata (Apis, Formica, etc.). (a) ,, entomophaga (Ichneumon, Platy gaster, etc). (3) ,, phytophaga ( Tenthredo, Sirex, etc.).
FlG. 177. TWO TRANSVERSE SECTIONS THROUGH
EMBRYOS OF HvDROPHiLUS piCEUS. (After Kowalevsky.)
A. Section through an embryo of the stage represented in fig. 176 B, at the point where the two germinal folds most approximate.
B. Section through an embryo somewhat later than the stage fig. 176 D, through the anterior region where the amnion has not completely closed over the embryo.
). The cells which form the floor of the groove are far more columnar than those of other parts of the blastoderm (fig. 177 A). The two folds on each side of it gradually approach each other. They do so at first behind, and then in the middle; from the latter point the approximation gradually extends backwards and forwards (fig. 176 B and C). In the middle and hinder parts of the ventral plate the groove becomes, by the coalescence of the folds, converted into a canal (fig. 178 A, gg), the central cavity of which soon disappears, while at the same time the cells of the wall undergo division, become more rounded, and form a definite layer (me} the mesoblast beneath the columnar cells of the surface. Anteriorly the process is slightly different, though it leads to the similar formation of mesoblast (fig. 177 B). The flat floor of the groove becomes in front bodily converted into the mesoblast, but the groove itself is never converted into a canal. The two folds simply meet above, and form a continuous superficial layer.
During the later stages of the process last described remarkable structures, eminently characteristic of the Insecta, have made their first appearance. These structures are certain embryonic membranes or coverings, which present in their mode of formation and arrangement a startling similarity to the true and false amnion of the Vertebrata. They appear as a double fold of the blastoderm round the edge of the germinal area, which spreads over the ventral plate, from behind forwards, in a
gg. germinal groove ; nion ; yk. yolk.
me. mesoblast ; am. am
general way in the same manner as the amnion in, for instance, the chick. The folds at their origin are shewn in surface view in fig. 176 D, am, and in section in fig. 177 B, am. The folds eventually meet, coalesce (fig. 178, am) and give rise to two membranes covering the ventral plate, viz. an inner one, which is continuous with the edge of the ventral plate ; and an outer, continuous with the remainder of the blastoderm. The vertebrate nomenclature may be conveniently employed for these membranes. The inner limb of the fold will therefore be spoken of as the amnion, and the outer one, including the dorsal part of the blastoderm, as the serous envelope 1 . A slight consideration of the mode of formation of the membranes, or an inspection of the figures illustrating their formation, makes it at once clear that the yolk can pass in freely between the amnion and serous envelope (vide fig. 181). At the hind end of the embryo this actually takes place, so that the ventral plate covered by the amnion appears to become completely imbedded in the yolk: elsewhere the two membranes are in contact. At first (fig. 176) the ventral plate occupies but a small portion of the ventral surface of the egg, but during the changes above described it extends over the whole ventral surface, and even slightly on the dorsal surface both in front and behind. It becomes at the same time (fig. 179) divided
FIG. 178. SECTIONS THROUGH TWO EMBRYOS OF HYDROPHILUS PICEUS. (After Kowalevsky.)
A. Section through the posterior part of the embryo fig. 1 76 D, shewing the completely closed amnion and the germinal groove.
B. Section through an older embryo in which the mesoblast has grown out into a continuous plate beneath the epiblast.
gg. germinal groove ; am. amnion ; yk. yolk ; cp. epiblast.
1 The reverse nomenclature to this is rather inconveniently employed by Metschnikoff.
FIG. 179. EMBRYO OF HYDROPHILUS PICEUS
VIEWED FROM THE VEN TRAL SURFACE. (After Kowalevsky.)
pc.L procephalic lobe.
by a series of transverse lines into segments, which increase in number and finally amount in all to seventeen, not including the most anterior section, which gives off as lateral outgrowths the two procephalic lobes (pc.l). The changes so far described are included within what Kowalevsky calls his first embryonic period; at its close the parts contained within the chorion have the arrangement shewn in fig. 178 B. The whole of the body of the embryo is formed from the ventral plate, and no part from the amnion or serous envelope.
The general history of the succeeding stages may be briefly told.
The appendages appear as very small rudiments at the close of the last stage, but soon become much more prominent (fig. 1 80 A). They are formed as outgrowths of both layers, and arise nearly simultaneously. There are in all eight pairs of appendages. The anterior or antennae (at) spring from the procephalic lobes, and the succeeding appendages from the segments following. The last pair of embryonic appendages, which disappears very early, is formed behind the third pair of the future thoracic limbs. Paired epiblastic involutions, shewn as pits in the posterior segments in fig. 1 80 A, give rise to the tracheae; and the nervous system is formed as two lateral epiblastic thickenings, one on each side of the midventral line. These eventually become split off from the skin ; while between them there passes in a median invagination of the skin
FlG. 1 80. TWO STAGES IN THE DEVELOPMENT OF HYDROPHILUS
PICEUS. (From Gegenbaur, after Kowalevsky.)
Is. labrum ; at. antenna ; md.
(fig. 189 C). The two nervous strands are continuous in front with the supra-oesophageal ganglia, which are formed of the epiblast of the procephalic lobes. These plates gradually grow round the dorsal side of the embryo, and there is formed immediately behind them an oral invagination, in front of which there appears an upper lip (fig. 180, Is). A proctodaeum is formed at the hind end of the body slightly later than the stomodaeum. The mesoblast cells become divided into two bands, one on each side of the middle line (fig. 189 A), and split into splanchnic and somatic layers. The central yolk mass at about the stage represented in fig. 179 begins to break up into yolk spheres. The hypoblast is formed first on the ventral side at the junction of the mesoblast and the yolk, and gradually extends and forms a complete sack-like mesenteron, enveloping the yolk (fig. 185 al). The amnion and serous membrane retain their primitive constitution for some time, but gradually become thinner on the ventral surface, where a rupture appears eventually to take place. The greater part of them disappears, but in the closure of the dorsal parietes the serous envelope plays a peculiar part, which is not yet understood. It is described on p. 404. The heart is formed from the mesoblastic layers, where they meet in the middle dorsal line (fig. 185 C, hi]. The somatic mesoblast gives rise to the muscles and connective tissue, and the splanchnic mesoblast to the muscular part of the wall of the alimentary tract, which accompanies the hypoblast in its growth round the yolk. The proctodaeum forms the rectum and Malpighian bodies 1 , and the stomodseum the oesophagus and proventriculus. The two epiblastic sections of the alimentary tract are eventually placed in communication with the mesenteron.
The development of Hydrophilus is a fair type of that of Insects generally, but it is necessary to follow with somewhat greater detail the comparative history of the various parts which have been briefly described for this type.
TJte embryonic membranes and the formation of the layers.
All Insects have at the close of segmentation a blastoderm formed of a single row of cells enclosing a central yolk mass,
1 This has not been shewn in the case of Hydrophilus,
which usually contains nuclei, and in the Poduridae is divided up in the ordinary segmentation into distinct yolk cells. The first definite structure formed is a thickening of the blastoderm, which forms a ventral plate.
The ventral plate is very differently situated in relation to the yolk in different types. In most Diptera, Hymenoptera and (?) Neuroptera (Phryganea) it forms from the first a thickening extending over nearly the whole ventral surface of the ovum, and in many cases extends in its subsequent growth not only over the whole ventral surface, but over a considerable part of the apparent dorsal surface as well (Chironomus, Simulia, Gryllotalpa, etc.). In Coleoptera, so far as is known, it commences as a less extended thickening either of the central part (Donacia) or posterior part (Hydrophilus) of the ventral surface, and gradually grows in both directions, passing over to the dorsal surface behind.
Embryonic membranes. In the majority of Insects there are developed enveloping membranes like those of Hydrophilus.
The typical mode of formation of these membranes is represented diagrammatically in fig. 181 A and B. A fold of the blastoderm arises round the edge of the ventral plate. This fold, like the amniotic fold of the higher Vertebrata, is formed of two limbs, an outer, the serous membrane (se), and an inner, the true amnion (am). Both limbs extend so as to cover over the ventral plate, and finally meet and coalesce, so thatadouble membrane is present over the ventral plate. At the same time (fig. 181 B) the point where the fold originates is carried dorsalwards by the B. II. 26
FIG. 181. DIAGRAMMATIC LONGITUDINAL SECTIONS OF AN INSECT EMBRYO AT TWO STAGES TO SHEW THE
DEVELOPMENT OF THE EMBRYONIC ENVELOPES.
In A the amniotic folds have not quite met so as to cover the ventral plate. The yolk is represented as divided into yolk cells. In B the sides of the ventral plate have extended so as nearly to complete the dorsal integument. The mesenteron is represented as a closed sack filled with yolk cells, am. amnion; se. serous envelope; v.p. ventral plate ; d. i. dorsal integument ; me. mesenteron ; st. stomodaeum ; an i. proctodaeum.
dorsal extension of the edges of the ventral plate, which give rise to the dorsal integument (d.i). This process continues till the whole dorsal surface is covered by the integument. The amnion then separates from the dorsal integument, and the embryo becomes enveloped in two membranes an inner, the amnion, and an outer, the serous membrane. In fig. 181 B the embryo is represented at the stage immediately preceding the closure of the dorsal surface.
By the time that these changes are effected, the serous membrane and amnion are both very thin and not easily separable. The amnion appears to be usually absorbed before hatching; but in hatching both membranes, if present, are either absorbed, or else ruptured and thrown off.
The above mode of development of the embryonic membranes has been especially established by the researches of Kowalevsky (No. 416) and Graber (No. 412) for various Hymenoptera (Apis), Diptera (Chironomus\ Lepidoptera and Coleoptera (Melolontha, Lino).
Considerable variations in the development of the enveloping membranes are known.
When the fold which gives rise to the membranes is first formed, there is, as is obvious in fig. 181 A, a perfectly free passage by which the yolk can pass in between the amnion and serous membrane. Such a passage of the yolk between the two membranes takes place posteriorly in Hydrophilus and Donacia: in Lepidoptera the yolk passes in everywhere, so that in this form the ventral plate becomes first of all imbedded in the yolk, and finally, on the completion of the dorsal integument, the embryo is enclosed in a complete envelope of yolk contained between the amnion and the serous membrane. During the formation of the dorsal integument the external yolk sack communicates by a dorsally situated umbilical canal with the yolk cavity within the body. On the rupture of the amnion the embryo is nourished at the expense of the yolk contained in the external yolk sack.
In the Hemiptera and the Libellulidae the ventral plate also becomes imbedded in the yolk, but in a somewhat different fashion to the Lepidoptera, which more resembles on an exaggerated scale what takes place in Hydrophilus.
In the Libellulidas (Calopteryx) there is first of all formed (Brandt, No. 403) a small ventral and posterior thickening of the blastoderm (fig. 182 A). The hinder part of this becomes infolded into the yolk as a projection (fig. 182 B), which consists of two laminae, an anterior and a posterior, continuous at the apex of the invagination. The whole structure, which is completely imbedded within the yolk, rapidly grows in length, and turns towards the front end of the egg (fig. 182 C). Its anterior lamina remains thick and gives rise to the ventral plate (ps), the posterior (am) on the other hand
becomes very thin, and forms a covering corresponding with the amnion of the more ordinary types. The remainder of the blastoderm covering the yolk (se) forms the homologue of the serous membrane of other types. The ventral surface of the ventral plate is turned towards the dorsal side (retaining the same nomenclature as in ordinary cases) of the egg, and the cephalic extremity is situated at the point of origin of the infolding.
The further history is however somewhat peculiar. The amnion is at first (fig. 182 C) continuous with the serous envelope on the posterior side only, so that the serous envelope does not form a continuous sack, but has an opening close to the head of the embryo. In the Hemiptera parasita this opening (Melnikow, No. 422) remains permanent, and the embryo, after it has reached a certain stage of development, becomes everted through it, while the yolk, enclosed in the continuous membrane formed by the amnion and serous envelope, forms a yolk sack on the dorsal surface. In the Libellulidae however and most Hemiptera, a fusion of the two limbs of the serous membrane takes place in the usual way, so as to convert it into a completely closed sack (fig. 183 A). After the formation of the appendages a fusion takes place between the amnion and serous envelope over a small area close to the head of the embryo. In the middle of this area a rupture is then effected, and the head of the embryo followed by the body is gradually pushed through the opening (fig. 183 B and C). The embryo becomes in the process completely rotated, and carried into a position in the egg-shell identical with that of the embryos of other orders of Insects (fig. 183 C).
Owing to the rupture of the embryonic envelopes taking place at the point where they are fused into one, the yolk does not escape in the above process, but is carried into a kind of yolk sack, on the dorsal surface of the embryo, formed of the remains of the amnion and serous envelope. The
FIG. 182. THREE STAGES IN THE DEVELOPMENT
OF THE EMBRYO OF CALOPTERYX. (After Brandt.)
The embryo is represented in the egg-shell.
A. Embryo with ventral plate.
B. Commencing involution of ventral plate.
C. Involution of ventral plate completed.
ps. vefitral plate; g. edge of ventral plate; am. amnion ; se- serous envelope.
walls of the yolk sack either assist in forming the dorsal parietes of the body, or are more probably enclosed within the body by the growth of the dorsal parietes from the edge of the ventral plate.
In Hydrophilus and apparently in the Phryganidae also, there are certain remarkable peculiarities in the closure of the dorsal surface. The fullest observations on the subject have been made by Kowalevsky (No. 416), but Dohrn (No. 408) has with some probability thrown doubts on Kowalevsky's interpretations. According to Dohrn the part of the serous envelope which covers the dorsal surface becomes thickened, and gives rise to a peculiar dorsal plate which is shewn in surface view in ventral parts of the amnion and serous membrane have either been ruptured or have disappeared. While the dorsal plate is being formed, the mesoblast, and somewhat later the lateral parts of the epiblast of the ventral plate gradually grow towards the dorsal side and enclose the dorsal plate, the wall of which in the process appears to be folded over so as first of all to form a groove and finally a canal. The stages in this growth are shewn from the surface in fig. 184 B and C and in section in
FlG. 183. THREE STAGES IN THE DEVELOPMENT
OF CALOPTERYX. (After Brandt.)
The embryo is represented in the egg-shell; B. and C. shew the inversion of the embryo.
sf. serous envelope ; am. amnion ; ab. abdomen ; v. anterior end of head ; at. antennae ; md. mandible ; mx l . maxilla i ; mx*. maxilla 2 ; p 1 ^. three pairs of legs; oe. oesophagus.
fig. 184 A, doi and in section in fig. 185 A, do. The
FIG. 184. THREE LARVAL STAGES OF HYDROPHILUS FROM THE DORSAL SIDE, SHEWING THE GRADUAL CLOSING IN OF THE DORSAL REGION WITH THE FORMATION < >! THK I'l.CULIAR DORSAL ORGAN
do. (After Kowalevsky.)
do. dorsal organ ; at. antennae.
fig. 185 B, do. The canal is buried on the dorsal part of the yolk, but for some time remains open by a round aperture in front (fig. 184 C). The whole structure is known as the dorsal canal. It appears to atrophy without leaving a trace. The heart when formed lies immediately dorsal to it 1 .
A. B. C.
FIG. 185. THREE TRANSVERSE SECTIONS THROUGH ADVANCED
EMBRYOS OF HYDROPHILUS.
Section through the posterior part of the body of the same age as fig. 184 A. Section through the embryo of the same age as fig. 184 C. Section through a still older embryo. do. dorsal plate ; vn. ventral nerve cord ; al. mesenteron ; ht. heart. The large spaces at the sides are parts of the body cavity.
In the Poduridas the embryonic membranes appear to be at any rate imperfect. Metschnikoff states in his paper on Geophilus that in some ants no true embryonic membranes are found, but merely scattered cells which take their place. In the Ichneumonidas the existence of two embryonic membranes is very doubtful.
Formation of the embryonic layers. The formation of the layers has been studied in sections by Kowalevsky (No. 416),
1 According to Kowalevsky the history of the dorsal plate is somewhat different. He believes that on the absorption of the amnion the ventral plate unites with the serous membrane, and that the latter directly gives rise to the dorsal integument, while the thickened part of it becomes involuted to form the dorsal tube already described.
Hatschek (No. 414), and Graber (No. 412), etc. From their researches it would appear that the formation of the mesoblast always takes place in a manner closely resembling that in Hydrophilus. The essential features of the process (figs. 177 and 178) appear to be that a groove is formed along the median line of the ventral plate, and that the sides of this groove either (i) simply close over like the walls of the medullary groove in Vertebrates, and so convert the groove into a tube, which soon becomes solid and forms a mass or plate of cells internal to the epiblast ; or (2) that the cells on each side of the groove grow over it and meet in the middle line, forming a layer external to the cells which lined the groove. The former of these processes is the most usual ; and in the Muscidae the dimensions of the groove are very considerable (Graber, No. 411). In both cases the process is fundamentally the same, and causes the ventral plate to become divided into two layers 1 . The external layer or epiblast is an uniform sheet forming the main part of the ventral plate (fig. 178 B, ep). It is continuous at its edge with the amnion. The inner layer or mesoblast constitutes an independent plate of cells internal to the epiblast (fig. 178 B, me). The mesoblast soon becomes divided into two lateral bands.
The origin of the hypoblast is still in dispute. It will be remembered (vide pp. 1 14 and 1 16) that after the segmentation a number of nuclei remain in the yolk ; and that eventually a secondary segmentation of the yolk takes place around these nuclei, and gives rise to a mass of yolk cells, which fill up the interior of the embryo. These cells are diagrammatically shewn in figs. 181 and 189, and it is probable that they constitute the true hypoblast. Their further history is given below.
Formation of the organs and their relation to the germinal
The segments and appendages. One of the earliest phenomena in the development is the appearance of transverse lines indicating segmentation (fig. 186). The transverse lines are apparently caused by shallow superficial grooves, and also in
1 Tichomiroff (No. 420) denies the existence of a true invagination to form the mesoblast, and also asserts that a separation of mesoblast cells from the epiblast can take place at other parts besides the median ventral line.
many cases by the division of the mesoblastic bands into separate somites. The most anterior line marks off a prae-oral segment, which soon sends out two lateral wings the procephalic lobes. The remaining segments are at first fairly uniform. Their number does not, however, appear to be very constant. So far as is known they never exceed seventeen, and this number is probably the typical one (figs. 186 and 187).
In Diptera the number appears to be usually fifteen though it may be only fourteen. In Lepidoptera and in Apis there appear to be sixteen segments. These and other variations affect only the number of the segments which form the abdomen of the adult.
The appendages arise as paired pouchlike outgrowths of the epiblast and mesoblast ; and their number and the order of their appearance are subject to considerable variation, the meaning of which is not yet clear. As a rule they arise subsequently to the segmentation of the parts of the body to which they belong. There is always formed one pair of appendages which spring from the lateral lobes of the procephalic region, or from the boundary line between these and the median ventral part of this region. These appendages are the antennae. They have in the embryo a distinctly ventral position as compared to that which they have in the adult.
In the median ventral part of the procephalic region there arises the labrum (fig. 187, Is}. It is formed by the coalescence of a pair of prominences very similar to true appendages, though it is probable that they have not this value 1 .
1 If these structures are equivalent to appendages, they may correspond to one of the pairs of antennae of Crustacea. From a figure by Fritz Miiller of the larva of Calotermes (Jenaische Zeit. Vol. XI. pi. n, fig. 12) it would appear that they lie in front of the true antennae, and would therefore on the above hypothesis correspond to the first pair of antennae of Crustacea. Biitschli (No. 405) describes in the Bee a pair of prominences immediately in front of the mandibles which eventually unite to form a kind of underlip ; they in some ways resemble true appendages.
FIG. 1 86. EMBRYO OF HYDROPHILUS PI CEUS VIEWED FROM THE VENTRAL SURFACE.
(After Kowalevsky.) pc. I. procephalic lobe.
The antennae themselves can hardly be considered to have the same morphological value as the succeeding appendages. They are rather equivalent to paired processes of the prae-oral lobes of the Chaetopoda.
From the first three post-oral segments there grow out the mandibles and two pairs of maxillae, and from the three following segments the three pairs of thoracic appendages. In many Insects (cf. Hydrophilus) a certain .number of appendages of the same nature as the anterior ones are visible in the embryo on the abdominal segments, a fact which shews that Insects are descended from ancestors with more than three pairs of ambulatory appendages.
In Apis according to Biitschli (No. 405) all the abdominal segments are provided with appendages, which always remain in a very rudimentary condition. All trace of them as well as of the thoracic appendages is lost by the time the embryo is hatched. In the phytophagous Hymenoptera the larva is provided with 9 ii pairs of legs.
In the embryo of Lepidoptera there would appear from Kowalevsky's figures to be rudiments of ten pairs of post-thoracic appendages. In the caterpillar of this group there are at the maximum five pairs of such rudimentary feet, viz. a pair on the 3rd, 4th, 5th, and 6th, and on the last abdominal segment. The embryos of Hydrophilus (fig. 187), Mantis, etc. are also provided with additional appendages. In various Thysanura small prominences are present on more or fewer of the abdominal segments (fig. 192), which may probably be regarded as rudimentary feet.
Whether all or any of the appendages of various kinds connected with the hindermost segments belong to the same category as the legs is very doubtful. Their usual absence in the embryo or in any case their late appearance appears to me against so regarding them ; but Biitschli is of opinion that in the Bee the parts of the sting are related genetically to the appendages of the penultimate and antepenultimate abdominal segments, and this view is to some extent supported by more recent
FlG. 187. TWO STAGES IN THE DEVELOPMENT OF HYDROPHILUS
PICEUS. (From Gegenbaur, after Kowalevsky. )
Is. labrum; at. antenna; tnd. mandible; nix. maxilla I.; li. maxilla II.; //>"/" feet; a. anus.
observations (Kraepelin, etc.), and if it holds true for the Bee must be regarded as correct for other cases also.
As to the order of the appearance of the appendages observations are as yet too scanty to form any complete scheme. In many cases all the appendages appear approximately at the same moment, e.g. Hydrophilus, but whether this holds good for all Coleoptera is by no means certain. In Apis the appendages are stated by Biitschli to arise simultaneously, but according to Kowalevsky the two mouth appendages first appear, then the antennae, and still later the thoracic appendages. In the Diptera the mouth appendages are first formed, and either simultaneously with these, or slightly later, the antennae. In the Hemiptera and Libellulidae the thoracic appendages are the first to be formed, and the second pair of maxillae makes its appearance before the other cephalic appendages.
The history of the changes in the embryonic appendages during the attainment of the 'adult con- .
dition is beyond the scope of this treatise, but it may be noted that the second pair of maxillae are relatively very large in the embryo, and not infrequently (Libellula, etc.) have more resemblance to the ambulatory than to the masticatory appendages.
The exact nature of the wings and their relation to the other segments is still very obscure. They appear as dorsal leaf-like appendages on the 2nd and 3rd thoracic segments, and are in many respects similar to the tracheal gills of the larvae of Ephemeridae and Phryganidae (fig. 1 88 A), of which they are supposed by Gegenbaur and Lubbock to be modifications. The undoubtedly secondary character of the closed tracheal system of larvae with tracheal gills tells against this view. Fritz Miiller finds in the larvae of Calotermes ru
FIG. 188. FIGURES ILLUSTRATING AQUATIC RESPIRATION IN INSECTS. (After Gegenbaur.)
A. Hinder portion of the body of Ephemera vulgata. a. longitudinal tracheal trunks; b. alimentary canal ; c. tracheal gills.
B. Larva of ^Eschna grandis. a. superior longitudinal tracheal trunks ; b. their anterior end ; c. portion branching on proctodaeum ; o. eyes.
C. Alimentary canal of the same larva from the side, a, b, and c. as in B ; d. inferior tracheal trunk ; e. transverse branches between upper and lower tracheal trunks.
gosus (one of the Termites) that peculiar and similar dorsal appendages are present on the two anterior of the thoracic segments. They are without tracheae. The anterior atrophies, and the posterior acquires tracheas and gives rise to the first pair of wings. The second pair of wings is formed from small processes on the third thoracic segment like those on the other two. Fritz Miiller concludes from these facts that the wings of Insects are developed from dorsal processes of the body, not equivalent to the ventral appendages. What the primitive function of these appendages was is not clear. Fritz Miiller suggests that they may have been employed as respiratory organs in the passage from an aqueous to a terrestrial existence, when the Termite ancestors lived in moist habitations a function for which processes supplied with blood-channels would be well adapted. The undoubted affinity of Insects to Myriapods, coupled with the discovery by Moseley of a tracheal system in Peripatus, is however nearly fatal to the view that Insects can have sprung directly from aquatic ancestors not provided with tracheae. But although this suggestion of Fritz Miiller cannot be accepted, it is still possible that the processes discovered by him may have been the earliest rudiments of wings, which were employed first as organs of propulsion by a water-inhabiting Insect ancestor which had not yet acquired the power of flying.
The nervous system. The nervous system arises entirely from the epiblast; but the development of the prae-oral and post-oral sections may be best considered separately.
The post-oral section, or ventral cord of the adult, arises as two longitudinal thickenings of the epiblast, one on each side of the median line (fig. 189 B, vn), which are subsequently split ofif from the superficial skin and give rise to the two lateral strands of the ventral cord. At a later period they undergo a differentiation into ganglia and connecting cords.
Between these two embryonic nerve cords there is at first a shallow furrow, which soon becomes a deep groove (fig. 189 C). At this stage the differentiation of the lateral elements into ganglia and commissures takes place, and, according to Hatschek (No. 414), the median groove becomes in the region of the ganglia converted into a canal, the walls of which soon fuse with those of the ganglionic enlargements of the lateral cords, and connect them across the middle line. Between the ganglia on the other hand the median groove undergoes atrophy, becoming first a solid cord interposed between the lateral strands of the nervous system, and finally disappearing without giving rise to any part of the nervous system. It is probable that Hatschek is entirely mistaken about the entrance of a median element into the ventral cord, and that the appearances he has described are due to shrinkage. In Spiders the absence of a median element can be shewn with great certainty, and, as already stated, this element is not present in
Peripatus. Hatschek states that in the mandibular segment the median element is absorbed, and that the two lateral cords of that part give rise to the oesophageal commissures, while the sub-cesophageal ganglion is formed from the fusion of the ganglia of the two maxillary segments.
The prae-oral portion of the nervous system consists entirely of the supra-cesophageal ganglion. It is formed, according to Hatschek, of three parts. Firstly and mainly, of a layer sepa
FIG. 189. THREE TRANSVERSE SECTIONS THROUGH THE EMBRYO OF HYDROPHILUS. (After Kowalevsky.)
A. Transverse section through the larva represented in fig. 187 A.
B. Transverse section through a somewhat older embryo in the region of one of the stigmata.
C. Transverse section through the larva represented in fig. 187 B.
vn. ventral nerve cord; am. amnion and serous membrane ; me. mesoblast ; me.s. somatic mesoblast ; hy. hypoblast (?) ; yk. yolk cells (true hypoblast) ; st. stigma of trachea.
rated from the thickened inner part of the cephalic lobe on each side ; secondly, of an anterior continuation of the lateral cords ; and thirdly, of a pit of skin invaginated on each side close to the
412 IN SECT A.
dorsal border of the antennae. This pit is at first provided with a lumen, which is subsequently obliterated; while the walls of the pit become converted into true ganglion cells. The two supra-cesophageal ganglia remain disconnected on the dorsal side till quite the close of embryonic life.
The tracheae and salivary glands. The tracheae, as was first shewn by Butschli (No. 405), arise as independent segmentally arranged paired invaginations of the epiblast (fig. 189 B and C, st). Their openings are always placed on the outer sides of the appendages of their segments, where such are present.
Although in the adult stigmata are never found in the space between the prothorax and head 1 , in the embryo and the larva tracheal invaginations may be developed in all the thoracic (and possibly in the three jaw-bearing segments) and in all the abdominal segments except the two posterior.
In the embryo of the Lepidoptera, according to Hatschek (No. 414), there are 14 pairs of stigmata, belonging to the 14 segments of the body behind the mouth ; but Tichomiroff states that Hatschek is in error in making this statement for the foremost post-oral segments. The last two segments are without stigmata. In the larvae of Lepidoptera as well as those of many Hymenoptera, Coleoptera and Diptera, stigmata are present on all the postcephalic segments except the 2nd and 3rd thoracic and the two last abdominal. In Apis there are eleven pairs of tracheal invaginations according to Kowalevsky (No. 416), but according to Butschli (No. 405) only ten, the prothorax being without one. In the Bee they appear simultaneously, and before the appendages.
The blind ends of the tracheal invaginations frequently (e.g. Apis) unite together into a common longitudinal canal, which forms a longitudinal tracheal stem. In other cases (eg. Gryllotalpa, Dohrn, No. 408) they remain distinct, and each tracheal stem has a system of branches of its own.
The development of the tracheae strongly supports the view, arrived at by Moseley from his investigations on Peripatus, that they are modifications of cutaneous glands.
The salivary and spinning glands are epiblastic structures, which in their mode of development are very similar to the tracheae, and perhaps have a similar origin. The salivary glands
1 In Smynthurus, one of the Collembola, there are, according to Lubbock, only two stigmata, which are placed on the head.
arise as paired epiblastic imaginations, not, as might be expected, of the Stomodaeum, but of the ventral plate behind the mouth on the inner side of the mandibles. At first independent, they eventually unite in a common duct, which falls into the mouth. The spinning glands arise on the inner side of the second pair of maxillae in Apis and Lepidoptera, and form elongated glands extending through nearly the whole length of the body. They are very similar in their structure and development to salivary glands, and are only employed during larval life. They no doubt resemble the mucous glands of the oral papillae of Peripatus, with which they have been compared by Moseley. The mucous glands of Peripatus may perhaps be the homologous organs of the first pair of maxillae, for the existence of which there appears to be some evidence amongst Insects.
Mesoblast. It has been stated that the mesoblast becomes divided in the region of the body into two lateral bands (fig. 189 A). These bands in many, if not all forms, become divided into a series of somites corresponding with the segments of the body. In each of them a cavity appears the commencing perivisceral cavity which divides them into a somatic plate in contact with the epiblast, and a splanchnic plate in contact with the hypoblast (fig. 189). In the interspaces between the segments the mesoblast is continuous across the median ventral line. The mesoblast is prolonged into each of the appendages as these are formed, and in the appendages there is present a central cavity. By Metschnikoff these cavities are stated to be continuous, as in Myriapods and Arachnida, with those of the somites ; but by Hatschek (No. 414) they are stated to be independent of those in the somites and to be open to the yolk.
The further details of the history of the mesoblast are very imperfectly known, and the fullest account' we have is that by Dohrn (No. 408) for Gryllotalpa. It would appear that the mesoblast grows round and encloses the dorsal side of the yolk earlier than the epiblast. In Gryllotalpa it forms a pulsating membrane. As the epiblast extends dorsalwards the median dorsal part of the membrane is constricted off as a tube which forms the heart. At the same time the free space between the pulsating membrane and the yolk is obliterated, but transverse passages are left at the lines between the somites, through which the blood passes from the ventral part of the body to corresponding openings in the wall of the heart. The greater part of the membrane gives rise to the muscles of the trunk.
Ventrally the mesoblastic bands soon meet across the median line. The cavities in the appendages become obliterated and their mesoblastic walls form the muscles, etc. The cavities in the separate mesoblastic somites also cease to be distinctly circumscribed.
The splanchnic mesoblast follows the hypoblast in its growth, and gives rise to the connective tissue and muscular parts of the walls of the alimentary tract. The mesoblastic wall of the proctodaeum is probably formed independently of the mesoblastic somites. In the head the mesoblast is stated to form at first a median ventral mass, which does not pass into the procephalic lobe ; though it assists in forming both the antennae and upper lip.
The alimentary canal. The alimentary tract of Insects is formed of three distinct sections (fig. 181) a mesenteron or middle section (me), a stomodaeum (st) and a proctodaeum (an). The stomodaeum and proctodaeum are invaginations of the epiblast, while the mesenteron is lined by the hypoblast. The distinction between the three is usually well marked in the adult by the epiblastic derivatives being lined by chitin. The stomodaeum consists of mouth, oesophagus, crop, and proventriculus or gizzard, when such are present. The mesenteron includes the stomach, and is sometimes (Orthoptera, etc.) provided at its front end with pyloric diverticula posteriorly it terminates just in front of the Malpighian bodies. These latter fall into the proctodaeum, which includes the whole of the region from their insertion to the anus.
The oral invagination appears nearly coincidently. with the first formation of segments at the front end of the groove between the lateral nerve cords, and the anal invagination appears slightly later at the hindermost end of the ventral plate.
The Malpighian bodies arise as two pairs of outgrowths of the epiblast of t/te proctodceum, whether solid at first is not certain. The subsequent increase which usually takes place in their number is due to sproutings (at first solid) of the two original vessels.
The glandular walls of the mesenteron are formed from the hypoblast ; but the exact origin of the layer has not been thoroughly worked out in all cases. In Hydrophilus it is stated by Kowalevsky (No. 416) to appear as two sheets split off from the lateral masses of mesoblast, which gradually grow round the yolk, and a similar mode of formation would seem to hold good for Apis. Tichomiroff (No. 420) confirms Kowalevsky on this point,
TR ACHE AT A. 415
and further states that these two masses meet first ventrally and much later on the dorsal side. In Lepidoptera, on the other hand, Hatschek finds that the hypoblast arises as a median mass of polygonal cells in the anterior part of the ventral plate. These cells increase by absorbing material from the yolk, and then gradually extend themselves and grow round the yolk.
Dohrn (No. 408) believes that the yolk cells, the origin of which has already been spoken of, give rise to the hypoblastic walls of the mesenteron, and this view appears to be shared by Graber (No. 412), though the latter author holds that some of the yolk cells are derived by budding from the blastoderm 1 .
From the analogy of Spiders I am inclined to accept Dohrn's and Graber's view. It appears to me probable that Kowalevsky's observations are to be explained by supposing that the hypoblast plates which he believes to be split off from the mesoblast are really separated from the yolk.
.It will be convenient to add here a few details to what has already been stated as to the origin of the yolk cells. As mentioned above, the central yolk breaks up at a period, which is not constant in the different forms, into polygonal or rounded masses, in each of which a nucleus has in many instances been clearly demonstrated although in others such nuclei have not been made out. It is probable however that nuclei are in all cases really present, and that these masses must be therefore regarded as cells. They constitute in fact the yolk cells. The periphery of the yolk breaks up into cells while the centre is still quite homogeneous.
The hypoblastic walls of the mesenteron appear to be formed in the first instance laterally (fig. 189 B and C, hy). They then meet ventrally (fig. 185 A and B), and finally close in the mesenteron on the dorsal side.
The mesenteron is at first a closed sack, independent of both stomodaeum and proctodaeum ; and in the case of the Bee it so remains even after the close of embryonic life. The only glandular organs of the mesenteron are the not unfrequent pyloric tubes, which are simple outgrowths of its anterior end. It is possible that in some instances they may be formed in situ around the lateral parts of the yolk.
In many instances the whole of the yolk is enclosed in the walls of the mesenteron, but in other cases, as in Chironomus and Simulia (Weismann, No. 430 ; Metschnikoff, No. 423), part of the yolk may be left between the ventral wall of the mesenteron and the ventral plate. In Chironomus the
1 Graber's view on this point may probably be explained by supposing that he has mistaken a passage of yolk cells into the blastoderm for a passage of blastoderm cells into the yolk. The former occurrence takes place, as I have found, largely in Spiders, and probably therefore also occurs in Insects.
41 6 INSECTA.
mass of yolk external to the mesenteron takes the form of a median and two lateral streaks. Some of the yolk cells either prior to the establishment of the mesenteron, or derived from the unenclosed portions of the yolk, pass into the developing organs (Dohrn, 408) and serve as a kind of nutritive cell. They also form blood corpuscles and connective-tissue elements. Such yolk cells may be compared to the peculiar bodies described by Reichenbach in Astacus, which form the secondary mesoblast. Similar cells play a very important part in the development of Spiders.
Generative organs. The observations on the development of the generative organs are somewhat scanty. In Diptera certain cells known as the pole cells are stated by both Metschnikoff (No. 423) and Leuckart to give rise to the generative organs. The cells in question (in Chironomus and Musca vomitoria, Weismann, No. 430) appear at the hinder end of the ovum before any other cells of the blastoderm. They soon separate from the blastoderm and increase by division. In the embryo, produced by the viviparous larva of Cecidomyia, there is at first a single pole cell, which eventually divides into four, and the resulting cells become enclosed within the blastoderm. They next divide into two masses, which are stated by Metschnikoff (No. 423) to become surrounded by indifferent embryonic cells 1 . Their protoplasm then fuses, and their nuclei divide, and they give rise to the larval ovaries, for which the enclosing cells form the tunics.
In Aphis Metschnikoff (No. 423) detected at a very early stage a mass of cells which give rise to the generative organs. These cells are situated at the hind end of the ventral plate ; and, except in the case of one of the cells which gives rise by division to a green mass adjoining the fat body, the protoplasm of the separate cells fuses into a syncytium. Towards the close of embryonic life the syncytium assumes a horse-shoe form. The mass is next divided into two, and the peripheral layer of each part gives rise to the tunic, while from the hinder extremity of each part an at first solid duct the egg- tube grows out. The masses themselves form the germogens. The oviduct is formed by a coalescence of the ducts from each germogen.
Ganin derives the generative organs in Platygaster (vide p. 347) from the hind end of the ventral plate close to the proctodaeum ; while Suckow states that the generative organs are outgrowths of the proctodicum. According to these two sets of observations the generative organs would appear to have an epiblastic origin an origin which is not incompatible with that from the pole cells.
In Lepidoptera the genital organs are present in the later periods of embryonic life as distinct paired organs, one on each side of the heart, in the eighth postcephalic segment. They are elliptical bodies with a duct passing off from the posterior end in the female or from the middle in the male. The egg-tubes or seminal tubes are outgrowths of the elliptical bodies.
1 This point requires further observation.
In other Insects the later stages in the development of the generative organs closely resemble those in the Lepidoptera, and the organs are usually distinctly visible in the later stages of embryonic life.
It may probably be laid down, in spite of some of Metschnikoff's observations above quoted, that the original generative mass gives rise to both the true genital glands and their ducts. It appears also to be fairly clear that the genital glands of both sexes have an identical origin.
Special types of larva.
Certain of the Hymenopterous forms, which deposit their eggs in the eggs or larvae of other Insects, present very peculiar modifications in their development. Platygaster, which lays its egg in the larvae of Cecidomyia, undergoes perhaps the most remarkable development amongst these forms. It has been studied especially by Ganin (No. 410), from whom the following account is taken.
The very first stages are unfortunately but imperfectly known, and the interpretations offered by Ganin do not in all cases appear quite satisfactory. In the earliest stage after being laid the egg is enclosed in a capsule produced into a stalk (fig. 190 A). In the interior of the egg there soon appears a single spherical body, regarded by Ganin as a cell (fig. 190 B). In the next stage three similar bodies appear in the vitellus, no doubt derived from the first one (fig. 190 C). The central one presents somewhat different characters to the two others, and, according to Ganin, gives rise to the whole embryo. The two peripheral bodies increase by division, and soon appear as nuclei imbedded in a layer of protoplasm (fig. 190 D, E, F). The layer so formed serves as a covering for the embryo, regarded by Ganin as equivalent to the amnion (? serous membrane) of other Insect embryos. In the embryo cell new cells are stated to be formed by a process of endogenous cell formation (fig. 190 D, E). It appears probable that Ganin has mistaken nuclei for cells in the earlier stages, and that a blastoderm is formed as in other Insects, and that this becomes divided in a way not explained into a superficial layer which gives rise to the serous envelope, and a deeper layer which forms the embryo. However this
B. II. 27
FlG. 190. A SERIES OF STAGES IN THE DEVELOPMENT
OF PLATYGASTER. (From Lubbock ; after Ganin.)
41 8 INSECTA.
may be, a differentiation into an epiblastic layer of columnar cells and a hypoblastic layer of more rounded cells soon becomes apparent in the body of the embryo. Subsequently to this the embryo grows rapidly, till by a deep transverse constriction on the ventral surface it becomes divided into an anterior cephalothoracic portion and a posterior caudal portion (fig. 190 F). The cephalothorax grows in breadth, and near its anterior end an invagination appears, which gives rise to the mouth and cesophagus. On the ventral side of the cephalothorax there is first formed a pair of claw-like appendages on each side of the mouth, then a posterior pair of appendages near the junction of the cephalothorax and abdomen, and lastly a pair of short conical antennae in front.
At the same time the hind end of the abdomen becomes bifid, and gives rise to a fork-like caudal appendage ; and at a slightly later period four grooves make their appearance in the caudal region, and divide this part of the embryo into successive segments. While these changes have been taking place in the general form of the embryo, the epiblast has given rise to a cuticle, and the hypoblastic cells have become differentiated into a central hypoblastic axis the mesenteron and a surrounding layer of mesoblast, some of the cells of which form longitudinal muscles.
With this stage closes what may be regarded as the embryonic development of Platygaster. The embryo becomes free from the amnion, and presents itself as a larva, which from its very remarkable characters has been spoken of as the Cyclops larva by Ganin.
The larvae of three species have been described by Ganin, which are represented in fig. 1 9 1 A, B, C. These larvae are strangely dissimilar to the ordinary Hexapod type, whether larval or adult. They are formed of a cephalothoracic shield with the three pairs of appendages (a, kf, lfg\ the development of which has already been described, and of an abdomen formed of five segments, the last of which bears the somewhat varying caudal appendages. The nervous system is as yet undeveloped.
The larvae move about in the tissues of their hosts by means of their claws.
The first larval condition is succeeded by a second with very different characters, and the passage from the first to the second is accompanied by an ecdysis.
The ecdysis commences at the caudal extremity, and the whole of the last segment is completely thrown off. As the ecdysis extends forwards the tail loses its segmentation and becomes strongly compressed, the appendages of the cephalothorax are thrown off, and the whole embryo assumes an oval form without any sharp distinction into different regions and without the slightest indication of segmentation (fig. 191 D). Of the internal changes which take place during the shedding of the cuticle, the first is the formation of a proctodaeum (gfi) by an invagination, which ends blindly in contact with the mesenteron. Shortly after this a thickening of the epiblast (bsm} appears along the ventral surface, which gives rise mainly to the ventral nerve cord ; this thickening is continuous behind with the
epiblast which is invaginated to form the proctodaeum, and in front is prolonged on each side into two procephalic lobes, in which there are also thickenings of the epiblast (gsae), which become converted into supraoesophageal ganglia, and possibly other parts.
Towards the close of the second larval period the muscles (/;) become segmentally arranged, and give indications of the segmentation which
FlG. 191. A SERIES OF STAGES IN THE DEVELOPMENT OF PLATYGASTER.
(From Lubbock ; after Ganin.)
A. B. C. Cyclops larvae of three species of Platygaster. D. Second larval stage. E. Third larval stage.
mo. mouth ; a. antenna ; kf. hooked feet ; Ifg. lateral feet ; /. branches of tail ; ul. lower lip ; slkf. oesophagus ; gsae. supra- oesophageal ganglion ; bsm. ventral epiblastic plate ; Im. lateral muscles (the letters also point in D to the salivary glands) ; gh. proctodseum ; ga. generative organs ; md. mandibles ; ag. ducts of salivary glands ; sp. (in E) salivary glands ; mis. stomach ; ed. intestine ; ew. rectum ; ao. anus ; tr. tracheae ; fk. fat body.
becomes apparent in the third larval period. The third and last larval stage (fig. 191 E) of Platygaster, during which it still remains in the tissues of its host, presents no very peculiar features. The passage from the second to the third form is accompanied by an ecdysis.
Remarkable as are the larvae just described, there can I think be no reason, considering their parasitic habits, for regarding them as ancestral.
Metamorphosis and heterogamy.
Metamorphosis. The majority of Insects are born in a condition in which they obviously differ from their parents. The extent of this difference is subject to very great variations, but as a rule the larvae pass through a very marked metamorphosis before reaching the adult state. The complete history of this metamorphosis in the different orders of Insects involves a far too considerable amount of zoological detail to be dealt with in this work ; and I shall confine myself to a few observations on the general characters and origin of the metamorphosis, and of the histological processes which take place during its occurrence 1 .
In the Aptera the larva differs from the adult only in the number of facets in the cornea and joints in the antennae.
In most Orthoptera and Hemiptera the larvae differ from the adult in the absence of wings and in other points. The wings, etc., are gradually acquired in the course of a series of successive moultings. In the Ephemeridae and Libellulidae, however, the metamorphosis is more complicated, in that the larvae have provisional tracheal gills which are exuviated before the final moult. In the Ephemeridae there are usually a great number of moultings ; the tracheal gills appear after the second moult, and the rudiments of the wings when the larva is about half grown. Larval life may last for a very long period.
In all the other groups of Insects, viz. the Diptera, Neuroptera, Coleoptera, Lepidoptera, and Hymenoptera, the larva passes with a few exceptions through a quiescent stage, in which it is known as a pupa, before it attains the adult stage. These forms are known as the Holometabola.
In the Diptera the larvae are apodous. In the true flies (Muscidae) they are without a distinct head and have the jaws replaced by hooks. In the Tipulidae there is on the other hand a well-developed head with the normal appendages. The pupae of the Muscidae are quiescent, and are enclosed in the skin of the larva which shrinks and forms a firm oval case. In the
1 For a systematic account of this subject the reader is referred to Lubbock (No. 420) and to Graber (No. 411). He will find in Weismann (Nos. 430 and 431) a detailed account of the internal changes which take place.
TRACHEATA. 42 1
Tipulidae the larval skin is thrown off at the pupa stage, and in some cases the pupae continue to move about.
The larvae of the Neuroptera are hexapodous voracious forms. When the larva becomes a pupa all the external organs of the imago are already established. The pupa is often invested in a cocoon. It is usually quiescent, though sometimes it begins to move about shortly before the imago emerges.
In the Coleoptera there is considerable variety in the larval forms. As a rule the larvae are hexapodous and resemble wingless Insects. But some herbivorous larvae (e.g. the larva of Melolontha) closely resemble true caterpillars, and there are also grub-like larvae without feet (Curculio) which resemble the larvae of Hymenoptera. The pupa is quiescent, but has all the parts of the future beetle plainly visible. The most interesting larvae among the Coleoptera are those of Sitaris, one of the Meloidae (Fabre, No. 409). They leave the egg as active hexapodous larvae which attach themselves to the bodies of Hymenoptera, and are thence transported to a cell filled with honey. Here they eat the ovum of the Hymenopterous form. They then undergo an ecdysis, in which they functionally lose their appendages, retaining however small rudiments of them, and become grubs. They feed on the honey and after a further ecdysis become pupae.
In the Lepidoptera the larva has the well-known form of a caterpillar. The caterpillars have strong jaws, adapted for biting vegetable tissues, which are quite unlike the oral appendages of the adult. They have three pairs of jointed thoracic legs, and a variable number (usually five) of pairs of rudimentary abdominal legs the so-called pro-legs. The larva undergoes numerous ecdyses, and the external parts of the adult such as the wings, etc., are formed underneath the chitinous exoskeleton before the pupa stage. The pupa is known as a chrysalis and in some Lepidoptera is enveloped in a cocoon.
The Hymenoptera present considerable variations in the character of the larvae. In the Aculeata, many Entomophaga, the Cynipidae, etc., the larvae are apodous grubs, incapable of going in search of their food ; but in the Siricidse they are hexapodous forms like caterpillars, which are sometimes even provided with pro-legs. In some of the Entomophaga the larvae have very remarkable characters which have already been described in a special section, 'vide pp. 418, 419.
Before proceeding to the consideration of the value of the various larval forms thus shortly enumerated, it is necessary to say a few words as to the internal changes which take place during the occurrence of the above metamorphosis. In the simplest cases, such as those of the Orthoptera and Hemiptera, where the metamorphosis is confined to the gradual formation of the wings, etc. in a series of moults, the wings first appear as two folds of the epidermis beneath the cuticle on the two posterior thoracic segments. At the next moult these processes
become covered by the freshly formed cuticle, and appear as small projections. At every successive moult these projections become more prominent owing to a growth in the epidermis which has taken place in the preceding interval. Accompanying the formation of such organs as the wings, internal changes necessarily take place in the arrangement of the muscles, etc. of the thorax, which proceed pari passu with the formation of the organs to which they belong. The characters of the metamorphosis in such forms as the Ephemeridae only differ from the above in the fact that provisional organs are thrown off at the same time that the new ones are formed.
In the case of the Holometabola the internal phenomena of the metamorphosis are of a very much more remarkable character. The details of our knowledge are largely due to Weismann (Nos. 430 and 431). The larvae of the Holometabola have for the most part a very different mode of life to the adults. A simple series of transitions between the two is impossible, because intermediate forms would be for the most part incapable of existing. The transition from the larval to the adult state is therefore necessarily a more or less sudden one, and takes place during the quiescent pupa condition. Many of the external adult organs are however formed prior to the pupa stage, but do not become visible on the surface. The simplest mode of Holometabolic metamorphosis may be illustrated by the development of Corethra plumicornis, one of the Tipulidae. This larva, like that of other Tipulidae, is without thoracic appendages, but before the last larval moult, and therefore shortly before the pupa stage, certain structures are formed, which Weismann has called imaginal discs. These imaginal discs are in Corethra simply invaginations of the epidermis. There are in the thorax six pairs of such structures, three dorsal and three ventral. The three ventral are attached to the terminations of the sensory nerves, and the limbs of the imago are formed as simple outgrowths of them, which as they grow in length take a spiral form. In the interior of these outgrowths are formed the muscles, tracheae, etc., of the limbs; which are believed by Weismann (it appears to me without sufficient ground) to be derived from a proliferation of the cells of the neurilemma. The wings are formed from the two posterior dorsal imaginal
discs. The hypodermis of the larva passes directly into that of the imago.
The pupa stage of Corethra is relatively very short, and the changes in the internal parts which take place during it are not considerable. The larval abdominal muscles pass for the most part unchanged into those of the imago, while the special thoracic muscles connected with the wings, etc., develop directly during the latest larval period from cords of cells already formed in the embryo.
In the Lepidoptera the changes in the passage from the larval to the adult state are not very much more considerable than those in Corethra. Similar imaginal discs give rise during the later larval periods to the wings, etc. The internal changes during the longer pupa period are somewhat more considerable. Important modifications and new formations arise in connection with the alimentary tract, the nervous and muscular systems.
The changes which take place in the true flies (Muscidse) are far more complicated than either those in Corethra or in the Lepidoptera. The abdomen of the larva of Musca becomes bodily converted into the abdomen of the imago as in the above types, but the whole epidermis and appendages of the head and thorax are derived from imaginal discs which are formed within and (so far as is known) independently of the epidermis of the larva or embryo. These imaginal discs are simple masses of apparently indifferent cells, which for the most part appear at the close of embryonic life, and are attached to nerves or tracheae. They grow in size during larval life, but during the relatively long pupa stage they unite together to give rise to a continuous epidermis, from which the appendages grow out as processes. The epidermis of the anterior part of the larva is simply thrown off, and has no share in forming the epidermis of the adult.
There are a pair of cephalic imaginal discs and six pairs of thoracic discs. Two pairs, a dorsal and a ventral, give rise to each thoracic ring, and the appendages attached to it.
Though, as mentioned above, no evidence has yet been produced to shew that the imaginal discs of Musca are derived from the embryonic epiblast, yet their mode of growth and
eventual fate proves beyond the shadow of a doubt that they are homologous with the imaginal discs of Corethra. Their earliest origin is well worth further investigation.
The metamorphosis of the internal organs is still more striking than that of the external. There is a disruption, total or partial, of all the internal organs except the generative organs. In the case of the alimentary tract, the Malpighian vessels, the heart and the central nervous system, the disruption is of a partial kind, which has been called by Weismann histolysis. The cells of these organs undergo a fatty degeneration, the nuclei alone in some cases remaining. The kind of plasma resulting from this degeneration retains the shape of the organs, and finally becomes built up again into the corresponding organs of the imago. The tracheae, muscles and peripheral nerves, and an anterior part of the alimentary tract, are entirely disrupted. They seem to be formed again from granular cells derived from the enormous fat body.
The phenomena of the development of the Muscidse are undoubtedly of rather a surprising character. Leaving for the moment the question of the origin of the pupa stage to which I return below, it will be admitted on all hands that during the pupa stage the larva undergoes a series of changes which, had they taken place by slow degrees, would have involved, in such a case as Musca, a complete though gradual renewal of the tissues. Such being the case, the cells of the organs common to the larva and the imago would, in the natural course of things, not be the same cells as those of the larva but descendants of them. We might therefore expect to find in the rapid conversion of the larval organs into those of the adult some condensation, so to speak, of the process of ordinary cell division. Such condensations are probably represented in the histolysis in the case of the internal organs, and in the formation of imaginal discs in the case of the external ones, and I think it probable that further investigation will shew that the imaginal discs of the Muscidae are derivatives of the embryonic epiblast. The above considerations by no means explain the whole of Weismann's interesting observations, but an explanation is I believe to be found by following up these lines.
More or less parallel phenomena to those in Insects are found in the development of the Platyelminthes and Echinoderms. The four disc-like invaginations of the skin in many larval Nemertines (vide p. 198), which give rise to the permanent body wall of the Nemertine, may be compared to the imaginal discs. The subsequent throwing off of the skin of Pilidium or larva of Desor is a phenomenon like the absorption of part of the larval skin of Musca. The formation of an independent skin within the first larval
TR ACHE AT A.
form in the Distomeaeand in the Cestoda may be compared to the apparently independent formation of the imaginal discs in Musca.
The fact that in a majority of instances it is possible to trace an intimate connection between the surroundings of a larva and its organization proves in the clearest way that the characters of the majority of existing larval forms of Insects have owed their origin to secondary adaptations. A few instances will illustrate this point.
In the simplest types of metamorphosis, e.g. those of the Orthoptera genuina, the larva has precisely the same habits as the adult. We find that a caterpillar form is assumed by phytophagous larvae amongst the Lepidoptera, Hymenoptera and Coleoptera. Where the larva has not to go in search of its nutriment the grub-like apodous form is assumed. The existence of such an apodous larva is especially striking in the Hymenoptera, in that rudiments of thoracic and abdominal appendages are present in the embryo and disappear again in the larva. The case of the larva of Sitaris, already described (p. 421), affords another very striking proof that the organization of the larva is adapted to its habits.
It follows from the above that the development of such forms as the Orthoptera genuina is more primitive than that of the holometabolous forms; a conclusion which tallies with the fact
HALF OF CAMPODEA FRAGILIS. (From Gegenbaur; after Palmen.)
a. antennae ; p. feet ; j> ', post-tho feet; s.
that both palaeontological and anatomical evidence shew the Orthoptera to be a very primitive group of Insects.
The above argument probably applies with still greater force to the case of the Thysanura ; and it seems to be probable that this group is more nearly related than any other to the primitive wingless ancestors of Insects 1 . The characters of the oral
1 Brauer and Lubbock (No. 421) have pointed out the primitive characters of these forms, especially of Campodea.
appendages in this group, the simplicity of their metamorphosis, and the presence of abdominal appendages (fig. 192), all tell in favour of this view, while the resemblance of the adult to the larvae of the Pseudoneuroptera, etc., points in the same direction. The Thysanura and Collembola are not however to be regarded as belonging to the true stock of the ancestors of Insects, but as degenerated relations of this stock ; much as Amphioxus and the Ascidians are degenerate relations of the ancestral stock of Vertebrates, and Peripatus of that of the Tracheata. It is probable that all these forms have succeeded in retaining their primitive characters from their degenerate habits, which prevented them from entering into competition in the struggle for existence with their more highly endowed relatives. While in a general way it is clear that the larval forms of Insects cannot be expected to throw much light on the nature of Insect ancestors, it does nevertheless appear to me probable that such forms as the caterpillars of the Lepidoptera are not without a meaning in this respect. It is easy to conceive that even a secondary larval form may have been produced by the prolongation of one of the embryonic stages ; and the general similarity of a caterpillar to Peripatus, and the retention by it of post-thoracic appendages, are facts which appear to favour this view of the origin of the caterpillar form.
The two most obscure points which still remain to be dealt with in the metamorphosis of Insects are (i) the origin of the quiescent pupa stage ; (2) the frequent dissimilarity between the masticatory apparatus of the larva and adult.
These two points may be conveniently dealt with together, and some valuable remarks about them will be found in Lubbock (No. 420).
On grounds already indicated it may be considered certain that the groups of Insects without a pupa stage, and with a larva very similarly organised to the adult, preceded the existing holometabolic groups. The starting-point in the metamorphosis of the latter groups was therefore something like that of the Orthoptera. Suppose it became an advantage to a species that the larva and adult should feed in a somewhat different way, a difference in the character of their mouth parts would soon make itself manifest ; and, since an intermediate type of mouth parts
would probably be disadvantageous, there would be a tendency to concentrate into a single moult the transition from the larval to the adult form of mouth parts. At each ordinary moult there is a short period of quiescence, and this period of quiescence would naturally become longer in the important moult at which the change in the mouth parts was effected. In this way a rudimentary pupa stage might be started. The pupa stage, once started, might easily become a more important factor in the metamorphosis. If the larva and imago diverged still more from each other, a continually increasing amount of change would have to be effected at the pupa stage. It would probably be advantageous to the species that the larva should not have rudimentary functionless wings ; and the establishment of the wings as external organs would therefore become deferred to the pupa stage. The same would probably apply to other organs.
Insects usually pass through the pupa stage in winter in cold climates and during the dry season in the tropics, this stage serving therefore apparently for the protection of the species during the inclement season of the year. These facts are easily explained on the supposition that the pupa stage has become secondarily adapted to play a part in the economy of the species quite different from that to which it owes its origin.
Heterogamy. The cases of alternations of generations amongst Insects all fall under the heading already defined in the introduction as Heterogamy. Heterogamy amongst Insects has been rendered possible by the existence of parthenogenesis, which, as stated in the introduction, has been taken hold of by natural selection, and has led to the production of generations of parthenogenetic forms, by which a clear economy in reproduction is effected. Parthenogenesis without heterogamy occurs in a large number of forms. In Bees, Wasps, and a Sawfly (Nematus ventricosus) the unfertilized ova give rise to males. In two Lepidopterous genera (Psyche and Solenobia) the unfertilized ova give rise mainly, if not entirely, to females. Heterogamy occurs in none of the above types, but in Psyche and Solenobia males are only occasionally found, so that a series of generations producing female young from unfertilized ova are followed by a generation producing young of both sexes from fertilized ova. It
would be interesting to know if the unimpregnated female would not after a certain number of generations give rise to both males and females ; such an occurrence might be anticipated on grounds of analogy. In the cases of true heterogamy parthenogenesis has become confined to special generations, which differ in their character from the generations which reproduce themselves sexually. The parthenogenetic generations generally flourish during the season when food is abundant; while the sexual generations occur at intervals which are often secondarily regulated by the season, supply of food, etc.
A very simple case of this kind occurs, if we may trust the recent researches of Lichtenstein 1 , in certain Gall Insects (Cynipidae). He finds that the female of a form known as Spathegaster baccarum, of which both males and females are plentiful, pricks a characteristic gall in certain leaves, in which she deposits the fertilized eggs. The eggs from these galls give rise to a winged and apparently adult form, which is not, however, Spathegaster, but is a species considered to belong to a distinct genus known as Neuroterus ventricularis. Only females of Neuroterus are found, and they lay unfertilized ova in peculiar galls which develop into Spathegaster baccarum. Here we have a true case of heterogamy, the females which produce parthenogenetically having become differentiated from those which produce sexually. Another interesting type of heterogamy is that which has been long known in the Aphides. In the autumn impregnated eggs are deposited by females, which give rise in the course of the spring to females which produce parthenogenetically and viviparously. The viviparous females always differ from the females which lay the fertilized eggs. The generative organs are of course differently constituted, and the ova of the viviparous females are much smaller than those of the oviparous females, as is generally the case in closely allied viviparous and oviparous forms; but in addition the former are usually without wings, while the latter are winged. The reverse is however occasionally the case. An indefinite number of generations of viviparous females may be produced if they are artificially kept warm and supplied with food ; but in the course of
1 Petites Nouvelles Entomolog iyues, May, 1878.
nature the viviparous females produce in the autumn males and females which lay eggs with firm shells, and so preserve the species through the winter. The heterogamy of the allied Coccidae is practically the same as that of the Aphidae. In the case of Chermes and Phylloxera the parthenogenetic generations lay their eggs in the normal way.
The complete history of Phylloxera quercus has been worked out by Balbiani (No. 401). The apterous females during the summer lay eggs developing parthenogenetically into apterous females, which continue the same mode of reproduction. In the autumn, however, the eggs which are laid give rise in part to winged forms and in part to apterous forms. Both of these forms lay smaller and larger eggs, which develop respectively into very minute males and females without digestive organs. The fertilized eggs laid by these forms probably give rise to the parthenogenetic females.
A remarkable case of heterogamy accompanied by paedogenesis was discovered by Wagner to take place in certain species of Cecydomyia (Miastor), a genus of the Diptera. The female lays a few eggs in the bark of trees, etc. These eggs develop in the winter into larvae, in which ovaries are early formed. The ova become detached into the body cavity, surrounded by their follicles, and grow at the cost of the follicles. They soon commence to undergo a true development, and on becoming hatched they remain for some time in the body cavity of the parent, and are nourished at the expense of its viscera. They finally leave the empty skin of their parent, and subsequently reproduce a fresh batch of larvae in the same way. After several generations the larvae undergo in the following summer a metamorphosis, and develop into the sexual form.
Another case of paedogenesis is that of the larvae of Chironomus, which have been shewn by Grimm (No. 413) to lay eggs which develop exactly in the same way as fertilized eggs into larvae.
(401) M. Balbiani. " Observations s. la reproduction d. Phylloxera du Chene." An. Sc. Nat. Ser. v. Vol. xix. 1874.
(402) E. Bess els. " Studien u. d. Entwicklung d. Sexualdriisen bei den Lepidoptera." Ztit.f. wiss. Zool. Bd. xvii. 1867.
(403) Alex. Brandt. "Beitrage zur Entwicklungsgeschichte d. Libellulida u. Hemiptera, mil besonderer Berucksichtigung d. Embryonalhiillen derselben." Mem. Ac. Petersbourg, Ser. vn. Vol. xm. 1869.
(404) Alex. Brandt. Ueber das Ei u. seine Bildungsstdttt. Leipzig, 1878.
(405) O. Biitschli. "Zur Entwicklungsgeschichte d. Biene." Zeit. f. wiss. Zool. Bd. xx. 1870.
(406) H. Dewitz. "Bau u. Entwicklung d. Stachels, etc." Zeit.f. wiss. Zool. Vols. xxv. and xxvin. 1875 and 1877.
(407) H. Dewitz. "Beitrage zur Kenntniss d. Postembryonalentwicklung d. Gliedmassen bei den Insecten." Zeit.f. wiss. Zool. xxx. Supplement. 1878.
(408) A. Dohrn. "Notizen zur Kenntniss d. Insectenentwicklung." Zeitschrift f. wiss. Zool. Bd. xxvi. 1876.
(409) M. Fabre. " L'hypermetamorphose et lesmoeursdes Meloides." An.Sci. Nat. Series iv. Vol. vn. 1857.
(410) Ganin. " Beitrage zur Erkenntniss d. Entwicklungsgeschichte d. Insecten." Zeit.f. wiss. Zool. Bd. xix. 1869.
(411) V. Graber. Die Insecten. MUnchen, 1877.
(412) V. Graber. "Vorlauf. Ergeb. lib. vergl. Embryologie d. Insecten." Archivf. mikr. Anat. Vol. XV. 1878.
(413) O. v. Grimm. " Ungeschlechtliche Fortpflanzung einer Chironomus Art-u. deren Entwicklung aus dem unbefruchteten Ei." Mem. Acad. Petersbourg. 1870.
(414) B. Hatschek. " Beitrage zur Entwicklung d. Lepidopteren." Jenaische Zeitschrift, Bd. XI.
(415) A. K 6 1 1 i k e r. " Observationes de prima insectorum genese, etc. " Ann. Sc. Nat. Vol. xx. 1843.
(416) A. Kowalevsky. " Embryologische Studien an Wurmern u. Arthropoden." Mem. Ac. imp. Petersbourg, Ser. vn. Vol. xvi. 1871.
(417) C. Kraepelin. 4 ' Untersuchungen Ub. d. Bau, Mechanismus u. d. Entwick. des Stachels d. bienartigen Thiere." Zeit.f. wiss. Zool. Vol. xxni. 1873.
(418) C. Kupffer. "Faltenblatt an d. Embryonen d. Gattung Chironomus." Arch.f. mikr. Anat. Vol. u. 1866.
(419) R. Leuckart. Zur Kenntniss d. Generationswechsels u. d. Parthenogenese b. d. Insecten. Frankfurt, 1858.
(420) Lubbock. Origin and Metamorphosis of Insects. 1874.
(421) Lubbock. Monograph on Collembola and Thysanura. Ray Society, 1873.
(422) Melnikow. " Beitrage z. Embryonalentwicklung d. Insecten." Archiv f. Naturgeschichte, Bd. xxxv. 1869.
(423) E. Metschnikoff. "Embryologische Studien an Insecten." Zeit. f. wiss. Zool. Bd. xvi. 1866.
(424) P. Meyer. "Ontogenie und Phylogenie d. Insecten." Jenaische Zeitschrift, Vol. x. 1876.
(425) FritzMiiller. " Beitrage z. Kenntniss d. Termiten." Jenaische Zeitschrift, Vol. IX. 1875.
(426) A. S. Packard. " Embryological Studies on Diplex, Perithemis, and the Thysanurous genus Isotoma." Mem. Peabody Acad. Science, I. i. 1871.
(427) Suckow. " Geschlechtsorgane d. Insecten." Ileusinger's Zeitschrift f. organ. Physik, Bd. n. 1828.
(428) Tichomiroff. " Ueber die Entwicklungsgeschichte des Seidenwiirms." Zoologischer Anzeiger, n. Jahr. No. 20 (Preliminary Notice).
(429) Aug. Weismann. "Zur Embryologie d. Insecten." Archiv f. Anat. und Phys. 1864.
(430) Aug. Weismann. " Entwicklung d. Dipteren." Zeit. f. wiss. Zool. Vols. xin. and xiv. Leipzig, 1863 4.
(431) Aug. Weismann. " Die Metamorphose d. Corethra plumicornis. " Zeit. f. wiss. Zool. Vol. xvi. 1866.
(432) N. Wagner. "Beitrag z. Lehre d. Fortpflanzung d. Insectenlarven." Zeit.f. wiss. Zool. Vol. xin. 1860.
(433) Zaddach. Untersuchungen iib. d. Bau u. d. Entwicklungd. Gliederthiere. Berlin, 1854.
ARACHNIDA 1 .
The development of several divisions of this interesting group has been worked out ; and it will be convenient to deal in the first instance with the special history of each of these divisions, and then to treat in a separate section the development of the organs for the whole group.
Scorpionidae. The embryonic development always takes place within the female Scorpion. In Buthus it takes place within follicle-like protuberances of the wall of the ovary. In Scorpio also development commences while the egg is still in the follicle, but when the trunk becomes segmented the embryo passes into the ovarian tube. The chief authority for the development of the Scorpionidae is Metschnikoff (No. 434).
At the pole of the ovum facing the ovarian tube there is
FIG. 193. OVUM OF SCORPION WITH THE ALREADY -FORMED BLASTODERM SHEWING THE PARTIAL SEGMENTATION. (After Metschnikoff.)
1 The classification of the Arachnida adopted in the present work is shewn below. c Scorpionidse. . . ( Tetrapneumones.
Pedipalpi. IL Aranema - JDipneumones.
I. ArthrOgastra. \ Pseudoscorpionidae.
I Soiifugse. in. Acarina,
formed a germinal disc which undergoes a partial segmentation (fig. 193 bl). A somewhat saucer-shaped one-layered blastoderm is then formed, which soon becomes thickened in the centre and then divided into two layers. The outer of these is the epiblast, the inner the mesoblast. Beneath the mesoblast there subsequently appear granular cells, which form the commencement of the hypoblast 1 .
During the formation of the blastoderm a cellular envelope is formed round the embryo. Its origin is doubtful, though it is regarded by Metschnikoff as probably derived from the blastoderm and homologous with the amnion of Insects. It becomes double in the later stages (fig. 195).
During the differentiation of the three embryonic layers the germinal disc becomes somewhat pyriform, the pointed end being the posterior. At this extremity there is a special thickening which is perhaps equivalent to the primitive cumulus of Spiders. The germinal disc continues gradually to spread over the yolk, but the original pyriform area is thicker than the remainder, and is marked off anteriorly and posteriorly by a shallow furrow. It constitutes a structure corresponding with the ventral plate of other Tracheata. It soon becomes grooved by a FIG. 194. THREE SURFACE VIEWS OF THE
. A ,. , f VENTRAL PLATE OF A DEVELOPING SCORPION.
shallow longitudinal fur- (After Metschnikoff.)
A. Before segmentation.
B. After five segments have become formed.
C. After the appendages have begun to be
row (fig. 194 A) which subsequently becomes less distinct. It is then divided by two transverse lines into three parts 2 .
1 The origin of the hypoblast cells, if such these cells are, is obscure. Metschnikoff doubtfully derives them from the blastoderm cells ; from my investigations on Spiders it appears to me more probable that they originate in the yolk.
- The exact fate of the three original segments is left somewhat obscure by
In succeeding stages the anterior of the three parts is clearly marked out as the procephalic lobe, and soon becomes somewhat broader. Fresh segments are added from before backwards, and the whole ventral plate increases rapidly in length (fig. 194 B).
When ten segments have become formed, appendages appear as paired outgrowths of the nine posterior segments (fig. 194 C). The second segment bears the pedipalpi, the four succeeding segments the four ambulatory appendages, and the four hindermost segments smaller provisional appendages which subsequently disappear, with the possible exception of the second. The foremost segment, immediately behind the procephalic lobes, is very small, and still without a rudiment of the chelicerae, which are subsequently formed on it. It would appear from Metschnikoff's figures to be developed later than the other post-oral segments present at this stage. The still unsegmented tail has become very prominent and makes an angle of 180 with the remainder of the body, over the ventral surface of which it is flexed.
By the time that twelve segments are definitely formed, the procephalic region is distinctly bilobed, and in the median groove extending along it the stomodaeum has become formed (fig. 196 A). The chelicerae (ck) appear as small rudiments on the first post-oral segment, and the
FlG. 195. A FAIRLY-ADVANCED EMBRYO OF THE SCORPION ENVELOPED IN
ITS MEMBRANES. (After Metschnikoff. )
ch. chelicerae ; pd. pedipalpi ; p^p 4 . ambulatory appendages ; al>. post-abdomen (tail).
Metschnikoff. He believes however that the anterior segment forms the procephalic lobes, the posterior probably the telson and five adjoining caudal segments, and the middle one the remainder of the body. This view does not appear to me quite satisfactory, since on the analogy of Spiders and other Arthropoda the fresh somites ought to be added by a continuous segmentation of the posterior lobe.
B. II. 28
434 1 SEUDOSCORPIONID^E.
nerve cords are distinctly differentiated and ganglionated. In the embryonic state there is one ganglion for each segment. The ganglion in the first segment (that bearing the chelicerse) is very small, but is undoubtedly post-oral.
At this stage, by a growth in which all the three germinal layers have a share, the yolk is completely closed in by the blastoderm. It is a remarkable fact with only few parallels, and those amongst the Arthropoda, that the blastopore, or point where the embryonic membranes meet in closing in the yolk, is situated on the dorsal surface of the embryo.
The general relations of the embryo at about this stage are shewn in fig. 195, where the embryo enclosed in its double cellular membrane is seen in a side view. This embryo is about the same age as that seen from the ventral surface in fig. 196 A.
The general nature of the further changes may easily be gathered from an inspection of fig. 196 B and C, but a few points may be noted.
An upper lip or labrum is formed as an unpaired organ in the line between the procephalic lobes. The pedipalpi become chelate before becoming jointed, and the chelicerae also early acquire their characteristic form. Rudimentary appendages appear on the six segments behind the ambulatory legs, five of which are distinctly shewn in fig. 195 ; they persist only on the second segment, where they appear to form the comb-like organs or pectines. The last abdominal segment, Le. that next the tail, is without provisional appendages. The embryonic tail is divided into six segments including the telson (fig. 196 C, ab). The lungs (st) are formed by paired invaginations, the walls of which subsequently become plicated, on the four last segments which bear rudimentary limbs, and simultaneously with the disappearance of the rudimentary limbs.
PseudoscorpionidaB. The development of Qielifer has been investigated by Metschnikoff (436), and although (except that it is provided with tracheae instead of pulmonary sacks) it might be supposed to be closely related to Scorpio, yet in its development is strikingly different.
The eggs after being laid are carried by the female attached to the first segment of the abdomen. The segmentation (vide p. 93) is intermediate between the types of complete and superficial segmentation. The ovum, mainly formed of food-yolk, divides into two, four, and eight equal segments
(fig. 197 A). There then appear one or more clear segments on the surface of these, and finally a complete layer of cells is formed round the central yolk spheres (fig. 197 B), which latter subsequently agglomerate into a central mass. The superficial cells form what may be called a blastoderm, which soon becomes divided into two layers (fig. 197 C). There now appears a single pair of appendages (the pedipalpi) (fig. 198 A,/^/), while at the same time the front end of the embryo grows out into a remarkable proboscis-like prominence a temporary upper lip (concealed in the figure
FIG. 196. THREE STAGES IN THE DEVELOPMENT OF THE SCORPION. THE
EMBRYOS ARE REPRESENTED AS IF SEEN EXTENDED ON A PLANE.
ch. chelicerae ; pd. pedipalpi ; p l />*. ambulatory appendages ; pe. pecten ; st. stigmata ; ab. post abdomen (tail).
behind the pedipalpus), and the abdomen (ab) becomes bent forwards towards the ventral surface. In this very rudimentary condition, after undergoing an ecdysis, the larva is hatched, although it still remains attached to its parent. After hatching it grows rapidly, and becomes filled with a peculiar transparent material. The first pair of ambulatory appendages is formed behind the pedipalpi and then the three suceeding pairs, while at the same time the chelicerae appear as small rudiments in front. External signs of segmentation have not yet appeared, but about this period the nervous system is formed. The supra-cesophageal ganglia are especially distinct, and provided with a central cavity, probably formed by an invagination, as in other Arachnida. In the succeeding stages (fig. 198 B) four provisional
pairs of appendages (shewn as small knobs at ati] appear behind the ambulatory feet. The abdomen is bent forwards so as to reach almost to the pedipalpi. In the later stages (fig. 198 C) the adult form is gradually attained. The enormous upper lip persists for some time, but subsequently atrophies and is replaced by a normal labrum. The appendages behind the
FIG. igj. SEGMENTATION AND FORMATION OF THE BLASTODERM IN CHELIFER.
In A the ovum is divided into a number of separate segments. In B a number of small cells have appeared (bl) which form a blastoderm enveloping the large yolk spheres. In C the blastoderm has become divided into two layers.
ambulatory feet atrophy, and the tail is gradually bent back into its final position. The segmentation and the gradual growth of the limbs do not call for special description, and the formation of the organs, so far as is known, agrees with other types.
The segmentation of Chthonius is apparently similar to that of Chelifer (Stecker, No. 437).
Phalangidae. Our knowledge of the development of Phalangium is unfortunately confined to the later stages (Balbiani, No. 438). These stages do not appear however to differ very greatly from those of true Spiders.
Araneina. The eggs of true Spiders are either deposited in nests made specially for them, or are carried about by the females. Species belonging to a considerable number of genera, viz. Pholcus, Epeira, Lycosa, Clubione, Tegenaria and Agelcna
have been studied by Claparede (No. 442), Balbiani (No. 439), Barrois (No. 441) and myself (No. 440), and the close similarity between their embryos leaves but little doubt that there are no great variations in development within the group.
The ovum is enclosed in a delicate vitelline membrane, enveloped in its turn by a chorion secreted by the walls of the oviduct. The chorion is covered by numerous rounded prominences, and occasionally exhibits a pattern corresponding with the areas of the cells which formed it. The segmentation has already been fully described, pp. 1 18 and 1 19. At its close there is present an enveloping blastoderm formed of a single layer of large flattened cells. The yolk within is formed of a number of
' r .v-ii~-cr^ ^H 1
FIG. 198. THREE STAGES IN THE DEVELOPMENT OF CHELIFKR.
(After Metschnikoff.) pd. pedipalpi ; ab. abdomen ; an.i. anal invagination ; c/i. chelicerse.
large polygonal segments ; each of which is composed of large yolk spherules, and contains a nucleus surrounded by a layer of protoplasm, which is prolonged into stellate processes holding together the yolk spherules. The nucleus, surrounded by the major part of the protoplasm of each yolk cell, appears, as a rule,
to be situated not at the centre, but on one side of its yolk segment.
The further description of the development of Spiders applies more especially to Agelena labyrinthica, the species which formed the subject of my own investigations.
The first differentiation of the blastoderm consists in the cells of nearly the whole of one hemisphere becoming somewhat more columnar than those of the other hemisphere, and in the cells of a small area near one end of the thickened hemisphere becoming distinctly more columnar than elsewhere, and two layers thick. This area forms a protuberance on the surface of the ovum, originally discovered by Claparede, and called by him the primitive cumulus. In the next stage the cells of the thickened hemisphere of the blastoderm become still more columnar; and a second area, at first connected by a whitish streak with the cumulus, makes its appearance. In the second area the blastoderm is also more than one cell deep (fig. 199). It will be noticed that the blastoderm, though more than one cell thick over a large part of the ventral surface, is not divided into distinct layers. The second area appears as a white patch and soon becomes more distinct, while the streak continued to it from the cumulus is no longer visible. It is shewn in surface view in fig. 200 A. Though my observations on this stage are not quite satisfactory, yet it appears to me probable that there is a longitudinal thickened ridge of the blastoderm extending from the primitive cumulus to the large white area. The section represented in fig. 199, which I believe to be oblique, passes through this ridge at its most projecting part.
The nuclei of the yolk cells during the above stages multiply rapidly, and cells are formed in the yolk which join the blastoderm ; there can however be no doubt that the main increase in the cells of the blastoderm has been due to the division of the original blastoderm cells.
In the next stage I have been able to observe there is, in the place of the previous thickened half of the blastoderm, a well developed ventral plate with a procephalic lobe in front, a caudal lobe behind, and an intermediate region marked by about three transverse grooves, indicating a division into segments. This plate is throughout two or more rows of
FIG. 199. SECTION THROUGH THE EMBRYO OF AGELENA LABYRINTHICA.
The section is from an embryo of the same age as fig. 200 A, and is represented with the ventral plate upwards. In the ventral plate is seen a keel-like thickening, which gives rise to the main mass of the mesoblast.
yk. yolk divided into large polygonal cells, in several of which nuclei are shewn.
cells thick, and the cells which form it are divided into two distinct layers a columnar superficial layer of epiblast cells, and a deeper layer of mesoblast cells (fig. 203 A). In the latter layer there are several very large cells which are in the act of passing from the yolk into the blastoderm. The identification of the structures visible in the previous stage with those visible in the present stage is to a great extent a matter of guess-work, but it appears to me probable that the primitive cumulus is still present as a slight prominence visible in surface views on the caudal lobe, and that the other thickened patch persists as the procephalic lobe. However this may be, the significance of the primitive cumulus appears to be that it is the part of the blastoderm where two rows of cells become first established \
The whole region of the blastoderm other than the ventral plate is formed of a single row of flattened epiblast cells. The yolk retains its original constitution.
By this stage the epiblast and mesoblast are distinctly differentiated, and the homologue of the hypoblast is to be sought for in the yolk-cells. The yolk-cells are not however entirely hypoblastic, since they continue for the greater part of the development to give rise to fresh cells which join the mesoblast.
The Spider's blastoderm now resembles that of an Insect (except for the amnion) after the establishment of the mesoblast, and the mode of origin of the mesoblast in both groups is very similar, in that the longitudinal ridge-like thickening of the
1 Various views have been put forward by Claparfede and Balbiani about the position and significance of the primitive cumulus. For a discussion of which vide self, No. 440.
mesoblast shewn in fig. 199 is probably the homologue of the mesoblastic groove of the Insects' blastoderm.
The ventral plate continues to grow rapidly, and at a somewhat later stage (fig. 200 B) there are six segments interposed between the procephalic and caudal lobes. The two anterior of these (ch and pd), especially the foremost, are less distinct than the remainder ; and it is probable that both of them, and in any case the anterior one, are formed later than the three segments following. These two segments are the segments of the chelicenc and pedipalpi. The four segments following belong to the four pairs of ambulatory legs. The segments form raised transverse bands separated by transverse grooves. There is at this stage a faintly marked groove extending along the median line of the ventral plate. This groove is mainly caused by the originally single mesoblastic plate having become divided throughout the whole region of the ventral plate, except possibly the procephalic lobes, into two bands, one on each side of the middle line (fig. 203 B).
The segments continue to increase in number by the continuous addition of fresh segments between the one last formed and the caudal lobe. By the stage with nine segments the first rudiments of the limbs make their appearance. The first rudiments to appear are those of the pedipalpi and four ambulatory limbs : the chelicerae, like the segment to which they belong, lag behind in development. The limbs appear as small protuberances at the borders of their segments. By the stage when they are formed the procephalic region has become bilobed, and the two lobes of which it is composed are separated by a shallow groove.
By a continuous elongation the ventral plate comes to form a nearly complete equatorial ring round the ovum, the procephalic and caudal lobes being only separated by a very narrow space, the undeveloped dorsal region of the embryo. This is shewn in longitudinal section in fig. 204. In this condition the embryo may be spoken of as having a dorsal flexure. By the time that this stage is reached (fig. 200 C) the full number of segments and appendages has become established. There are in all sixteen segments (including the caudal lobe). The first six of these bear the permanent appendages of the adult ; the
next four are provided with provisional appendages ; while the last six are without appendages. The further features of this stage which deserve notice are (i) the appearance of a shallow depression (st) the rudiment of the stomodaeum between the hinder part of the two procephalic lobes ; (2) the appearance of
FIG. aoo. FOUR STAGES IN THE DEVELOPMENT OF AGELENA LABYRINTHICA.
A. Stage when the ventral plate is very imperfectly differentiated, pr.c. primitive cumulus.
B. Ovum viewed from the side when the ventral plate has become divided into six segments, ch. segment of chelicerae imperfectly separated from procephalic lobe ; pd. segment of pedipalpi.
C. Ventral plate ideally unrolled after the full number of segments and appendages are established, st. stomodoeum between the two proe-oral lobes. Behind the six pairs of permanent appendages are seen four pairs of provisional appendages.
D and E. Two views of an embryo at the same stage. D ideally unrolled, E seen from the side. st. stomodseum ; ch. chelicerse ; on their inner side is seen the ganglion belonging to them. pd. pedipalpi ; pr.p. provisional appendages.
raised areas on the inner side of the six anterior appendagebearing segments. These are the rudiments of the ventral ganglia. It deserves to be especially noted that the segment of
44 2 AKANEINA.
the chelicera, like the succeeding segments, is provided with ganglia ; and that the ganglia of the chelicerae are quite distinct from the supra-cesophageal ganglia derived from the procephalic lobes. (3) The pointed form of the caudal lobe. In Pholcus (Claparede, No. 442) the caudal lobe forms a projecting structure which, like the caudal lobe of the Scorpion, bends forward so as to face the ventral surface of the part of the body immediately in front. In most Spiders such a projecting caudal lobe is not found. While the embryo still retains its dorsal flexure considerable changes are effected in its general constitution. The appendages (fig. 200 D and E) become imperfectly jointed, and grow inwards so as to approach each other in the middle line. Even in the stage before this, the ventral integument between the rudiments of the ganglia had become very much thinner, and had in this way divided the ventral plate into two halves. At the present stage the two halves of the ventral plate are still further separated, and there is a wide space on the ventral side only covered by a delicate layer of epiblast. This is shewn in surface view (fig. 200 D) and in section in fig. 203 C.
The stomodaeum (j/) is much more conspicuous, and is bounded in front by a prominent upper lip, and by a less marked lip behind. The upper lip becomes less conspicuous in later stages, and is perhaps to be compared with the provisional upper lip of Chelifer. Each procephalic lobe is now marked by a deep semicircular groove.
The next period in the development is characterised by the gradual change in the flexure of the embryo from a dorsal to a ventral one ; accompanied by the division of the body into an abdomen and cephalo-thorax, and the gradual assumption of the adult characters.
The change in the flexure of the embryo is caused by the elongation of the dorsal region, which has hitherto been hardly developed. Such an elongation increases the space on the dorsal surface between the procephalic and caudal regions, and therefore necessarily separates the caudal and procephalic lobes ; but, since the ventral plate does not become shortened in the process, and the embryo cannot straighten itself in the egg-shell, it necessarily becomes ventrally flexed.
If there were but little food yolk this flexure would naturally
cause the whole embryo to be bent in so as to have the ventral surface concave. But instead of this the flexure is at first confined to the two bands which form the ventral plate. These bands, as shewn in fig. 201 A, acquire a true ventral flexure, but the yolk forms a projection a kind of yolk sack as Barrois (No. 441) calls it distending the thin integument between the two ventral bands. This yolk sack is shewn in surface view in
FlG. 201. TWO LATE STAGES IN THE DEVELOPMENT OF AGELENA LABYRINTHICA.
A. Embryo from the side at the stage when there is a large ventral protuberance of yolk. The angle between the line of insertion of the permanent and provisional appendages shews the extent of the ventral flexure.
B. Embryo nearly ready to be hatched. The abdomen which has not quite acquired its permanent form is seen to be pressed against the ventral side of the thorax.
prJ. procephalic lobe; pd. pedipalpi ; ch. chelicerae ; c,L caudal lobe; pr.p. provisional appendages.
fig. 20 1 A and in section in fig. 206. At a later period, when the yolk has become largely absorbed, the true nature of the ventral flexure becomes quite obvious, since the abdomen of the young Spider, while still in the egg, is found to be bent over so as to press against the ventral surface of the thorax (fig. 201 B). The general character of the changes which take place during this period in the development is shewn in fig. 201 A and B representing two stages in it. In the first of these stages there is no constriction between the future thorax and abdomen.
The four pairs of provisional appendages exhibit no signs of atrophy ; and the extent of the ventral flexure is shewn by the angle formed between the line of their insertion and that of the appendages in front. The yolk has enormously distended the integument between the two halves of the ventral plate, as is illustrated by the fact that, at a somewhat earlier stage than that figured, the limbs cross each other in the median ventral line, while at this stage they do not nearly meet The limbs have acquired their full complement of joints, and the pedipalpi bear a cutting blade on their basal joint.
The dorsal surface between the prominent caudal lobe and the procephalic lobes forms more than a semicircle. The terga are fully established, and the boundaries between them, especially in the abdomen, are indicated by transverse markings. A large lower lip now bounds the stomodaeum, and the upper lip has somewhat atrophied. In the later stage (fig. 201 B) the greater part of the yolk has passed into the abdomen, which is now to some extent constricted off from the cephalo-thorax. The appendages of the four anterior abdominal somites have disappeared, and the caudal lobe has become very small. In front of it are placed two pairs of spinning mammillae. A delicate cuticle has become established, which is very soon moulted.
Acarina. The development of the Acarina, which has been mainly investigated by Claparede (No. 446), is chiefly remarkable from the frequent occurrence of several larval forms following each other after successive ecdyses. The segmentation (vide p. 116) ends in the formation of a blastoderm of a single layer of cells enclosing a central yolk mass.
A ventral plate is soon formed as a thickening of the blastoderm, in which an indistinct segmentation becomes early observable. In Myobia, which is parasitic on the common mouse, the ventral plate becomes divided by five constrictions into six segments (fig. 202 A), from the five anterior of which paired appendages very soon grow out (fig. 202 B) The appendages are the chelicerae (ch} and pedipalpi (pd] and the first three pairs of limbs (p^fi 1 }. On the dorsal side of the chelicerae a thickened prominence of the ventral plate appears to correspond to the procephalic lobes of other Arachnida. The part of the body behind the five primitive appendage-bearing segments appears to become divided into at least two segments. In other mites the same appendages are formed as in Myobia, but the preceding segmentation of the ventral plate is not always very obvious.
In Myobia two moultings take place while the embryo is still within the primitive egg-shell. The first of these is accompanied by the apparently total disappearance of the three pediform appendages, and the complete
TRACK EAT A.
coalescence of the two gnathiform appendages into a proboscis (fig. 202 C). The feet next grow out again, and a second ecdysis then takes place. The embryo becomes thus inclosed within three successive membranes, viz. the original egg-shell and two cuticular membranes (fig. 202 D). After the second ecdysis the appendages assume their final form, and the embryo leaves the egg as an hexapodous larva. The fourth pair of appendages is
FIG. 202. FOUR SUCCESSIVE STAGES IN THE DEVELOPMENT OF MYOBIA MUSCULI. (After Claparede.)
J 1 j 4 . post-oral segments ; ch. chelicerae ; pd. pedipalpi ; pr. proboscis formed by the coalescence of the chelicerse and pedipalpi ; p l , /*, etc. ambulatory appendages.
acquired by a post-embryonic metamorphosis. From the proboscis are formed the rudimentary palpi of the second pair of appendages, and two elongated needles representing the chelicerae.
In the cheese mite (Tyroglyphus) the embryo has two ecdyses which are not accompanied by the peculiar changes observable in Myobia : the cheliceras and pedipalpi fuse however to form the proboscis. The first larval form is hexapodous, and the last pair of appendages is formed at a subsequent ecdysis.
In Atax Bonzi, a form parasitic on Unio, the development and metamorphosis are even more complicated than in Myobia. The first ecdysis occurs before the formation of the limbs, and shortly after the ventral plate has become divided into segments. Within the cuticular membrane resulting from the first ecdysis the anterior five pairs of limbs spring out in the usual fashion. They undergo considerable differentiation ; the chelicerae and pedipalpi approaching each other at the anterior extremity of the body, and the three ambulatory legs becoming segmented and clawed. An oesophagus, a stomach, and an oesophageal nerve-ring are also formed. When the larva
has attained this stage the original egg-shell is split into two valves and eventually cast off, but the embryo remains enclosed within the cuticular membrane shed at the first ecdysis. This cuticular membrane is spoken of by Claparede as the deutovum. In the deutovum the embryo undergoes further changes ; the chelicerae and pedipalpi coalesce and form the proboscis ; a spacious body cavity with blood corpuscles appears ; and the alimentary canal enclosing the yolk is formed.
The larva now begins to move, the cuticular membrane enclosing it is ruptured, and the larva becomes free. It does not long remain active, but soon bores its way into the gills of its host, undergoes a fresh moult, and becomes quiescent. The cuticular membrane of the moult just effected swells up by the absorption of water and becomes spherical. Peculiar changes take place in the tissues, and the limbs become, as in Myobia, nearly absorbed, remaining however as small knobs. The larva swims about as a spherical body within its shell. The feet next grow out afresh, and the posterior pair is added. From the proboscis the palpi (of the pedipalpi) grow out below. The larva again becomes free, and amongst other changes the chelicerae grow out from the proboscis. A further ecdysis, with a period of quiescence, intervenes between this second larval form and the adult state.
The changes in the appendages which appear common to the Mites generally are (i) the late development of the fourth pair of appendages, which results in the constant occurrence of an hexapodous larva ; and (2) the early fusion of the chelicerae and pedipalpi to form a proboscis in which no trace of the original appendages can be discerned. In most instances palpi and stilets of variable form are subsequently developed in connexion with the proboscis, and, as indicated in the above descriptions, are assumed to correspond with the two original embryonic appendages.
TJie history of tJie germinal layers.
It is a somewhat remarkable fact that each of the groups of the Arachnida so far studied has a different form of segmentation. The types of Chelifer and the Spiders are simple modifications of the centrolecithal type, while that of Scorpio, though apparently meroblastic, is probably to be regarded in the same light (vide p. 120 and p. 434). The early development begins in the Scorpion and Spiders with the formation of a ventral plate, and there can be but little doubt that Chelifer is provided with an homologous structure, though very probably modified, owing to the small amount of food-yolk and early period of hatching.
The history of the layers and their conversion into the organs has been studied in the case of the Scorpion (Metschnikoff, No.
434), and of the Spiders ; and a close agreement has been found to obtain between them.
It will be convenient to take the latter group as type, and simply to call attention to any points in which the two groups differ.
The epiblast. The epiblast, besides giving rise to the skin (hypodermis and cuticle), also supplies the elements for the nervous system and organs of sense, and for the respiratory sacks, the stomodaeum and proctodaeum.
At the period when the mesoblast is definitely established, the epiblast is formed of a single layer of columnar cells in the region of the ventral plate, and of a layer of flat cells over other parts of the yolk.
When about six segments are present the first changes take place. The epiblast of the ventral plate then becomes somewhat thinner in the median line than at the two sides (fig. 203 B). In succeeding stages the contrast between the median and the lateral parts becomes still more marked, so that the epiblast becomes finally constituted of two lateral thickened bands, which meet in front in the procephalic lobes, and behind in the caudal lobe, and are elsewhere connected by a very thin layer (fig. 203 C). Shortly after the appendages begin to be formed, the first rudiments of the ventral nerve-cord become established as epiblastic thickenings on the inner side of each of the lateral bands. The thickenings of the epiblast of the two sides are quite independent, as may be seen in fig. 203 C, vn, taken from a stage somewhat subsequent to their first appearance. They are developed from before backwards, but either from the first, or in any case very soon afterwards, cease to form uniform thickenings, but constitute a linear series of swellings the future ganglia connected by very short less prominent thickenings of the epiblast (fig. 200 C). The rudiments of the ventral nerve-cord are for a long time continuous with the epiblast, but shortly after the establishment of the dorsal surface of the embryo they become separated from the epiblast and constitute two independent cords, the histological structure of which is the same as in other Tracheata (fig. 206, vn\
The ventral cords are at first composed of as many ganglia as there are segments. The foremost pair, belonging to the
segment of the chelicerae, lie immediately behind the stomodaeum, and are as independent of each other as the remaining ganglia. Anteriorly they border on the supra-cesophageal ganglia. When the yolk sack is formed in connection with the ventral flexure of the embryo, the two nerve-cords become very widely separated (fig. 206, vn) in their middle region. At a later period, at the stage represented in fig. 201 B, they again become approximated in the ventral line, and delicate commissures are formed uniting
FIG. 203. TRANSVERSE SECTIONS THROUGH THE VENTRAL PLATE OF AGELBNA LABYRINTHICA AT THREE STAGES.
A. Stage when about three segments are formed. The mesoblastic plate is not divided into two bands.
B. Stage when six segments are present (fig. ?oo B). The mesoblast is now divided into two bands.
C. Stage represented in fig. 200 D. The ventral cords have begun to be formed on thickenings of the epiblast, and the limbs are established.
ep. epiblast ; me. mesoblast ; me.s. mesoblastic somite ; 7>n. ventral nerve-cord ; yk. yolk.
the ganglia of the two sides, but there is no trace at this or any other period of a median invagination of epiblast between the two cords, such as Hatschek and other observers have attempted to establish for various Arthropoda and Chaetopoda. At the stage represented in fig. 201 A the nerve ganglia are still present in the abdomen, though only about four ganglia can be distinguished. At a later stage these ganglia fuse into two continuous
cords, united however by commissures corresponding with the previous ganglia.
The ganglia of the chelicerae have, by the stage represented in fig. 20 1 B, completely fused with the supra-oesophageal ganglia and form part of the oesophageal commissure. The cesophageal commissure is however completed ventrally by the ganglia of the pedipalpi.
The supra-cesophageal ganglia are formed independently of the ventral cords as two thickenings of the procephalic lobes (fig. 205). The thickenings of the two lobes are independent, and each of them becomes early marked out by a semicircular groove (fig. 200 D) running outwards from the upper lip. Each thickening eventually becomes detached from the superficial epiblast, but before this takes place the two grooves become deeper, and on the separation of the ganglia from the epiblast, the cells lining the grooves become involuted and detached from the skin, and form an integral part of the supra-oesophageal ganglia.
At the stage represented in fig. 201 B the supra-oesophageal ganglia are completely detached from the epiblast, and are constituted of the following parts : (i) A dorsal section formed of two hemispherical lobes, mainly formed of the invaginated lining of the semicircular grooves. The original lumen of the groove is still present on the outer side of these lobes. (2) Two central masses, one for each ganglion, formed of punctiform tissue, and connected by a transverse commissure. (3) A ventral anterior lobe. (4) The original ganglia of the chelicerae, which form the ventral parts of the ganglia 1 .
The later stages in the development of the nervous system have not been worked out.
The development of the nervous system in the Scorpion is almost identical with that in Spiders, but Metschnikoff believes, though without adducing satisfactory evidence, that the median integument between the two nerve cords assists in forming the ventral nerve cord. Grooves are present in the supra-cesophageal ganglia similar to those in Spiders.
The mesoblast. The history of the mesoblast, up to the formation of a ventral plate subjacent to the thickened plate of epiblast, has been already given. The ventral plate is shewn in fig. 203 A. It is seen to be formed mainly of small cells,
1 For further details vide self, No. 440. B. II. 29
but some large cells are shewn in the act of passing into it from the yolk. During a considerable section of the subsequent development the mesoblast is confined to the ventral plate.
The first important change takes place when about six somites are established ; the mesoblast then becomes divided
FIG. 204. LONGITUDINAL SECTION THROUGH AN EMBRYO OF AGELENA
The section is through an embryo of the same age as that represented in fig. 200 C, and is taken slightly to one side of the middle line so as to shew the relation of the mesoblastic somites to the limbs. In the interior are seen the yolk segments and their nuclei.
i 16. the segments; pr.l. procephalic lobe ; do. dorsal integument.
into two lateral bands, shewn in section in fig. 203 B, which meet however in front in the procephalic lobes, and behind in the caudal lobes. Very shortly afterwards these bands become broken up into a number of parts corresponding to the segments, each of which soon becomes divided into two layers, which enclose a cavity between them (vide fig. 204 and fig. 207). The outer layer (somatic) is thicker and attached to the epiblast, and the inner layer (splanchnic) is thinner and mainly, if not entirely, derived (in Agelena) from cells which originate in the yolk. These structures constitute the mesoblastic somites. In the appendage-bearing segments the somatic layer of each of them, together with a prolongation of the cavity, is continued
into the appendage (fig. 203 C). Since the cavity of the mesoblastic somites is part of the body cavity, all the appendages contain prolongations of the body cavity. Not only is a pair of mesoblastic somites formed for each segment of the body, but also for the procephalic lobes (fig. 205). The mesoblastic somites for these lobes are established somewhat later than for the true segments, but only differ from them in the fact that the somites of the two sides are united by a median bridge of undivided mesoblast. The development of a somite for the procephalic lobes is similar to what has been described by Kleinenberg for Lumbricus (p. 339), but must not be necessarily supposed to indicate that the procephalic lobes form a segment equivalent to the segments of the trunk. They are -rather equivalent to the
FIG. 205. SECTION THROUGH THE PROCEPHALIC LOBES OF AN EMBRYO OF AGELENA LABYRINTHICA.
The section is taken from an embryo of the same age as fig. 200 D.
Drae oral lobe of g roove
stomodseum ; gr. section through semi-circular procephalic lobe ; ce.s. cephalic section of body cavitv.
Chaetopod larvae. When the dorsal surface of the embryo is established a thick layer of mesoblast becomes formed below the epiblast. This layer is not however derived from an upgrowth of the mesoblast of the somites, but from cells which originate in the yolk. The first traces of the layer are seen in fig. 204, do, and it is fully established as a layer of large round cells in the stage shewn in fig. 206. This layer of cells is seen to be quite independent of the mesoblastic somites (ine.s). The mesoblast of the dorsal surface becomes at the stage represented in fig. 201 B divided into splanchnic and somatic layers, and in the abdomen at any rate into somites continuous with those of the ventral part of the mesoblast. At the lines of junction of successive somites the splanchnic layer of mesoblast dips into the yolk, and forms a number of transverse septa, which do not reach the middle of the yolk, but leave a central part free, in which the mesenteron is subsequently formed. At the insertion of these septa there
are developed widish spaces between the layers of somatic and splanchnic mesoblast, which form transversely directed channels passing from the heart outwards. They are probably venous. At a later stage the septa send out lateral offshoots, and divide the peripheral part of the abdominal cavity into a number of compartments filled with yolk. It is probable that the hepatic diverticula are eventually formed in these compartments.
The somatic layer of mesoblast
FIG. 206. TRANSVERSE SECTION THROUGH THE THORACIC REGION OF AN EMBRYO OF AGELENA LABYRINTHICA.
The section is taken from an embryo of the same age as fig. 201 A, and passes through the maximum protuberance of the ventral yolk sack.
vn. ventral nerve cord ; yk. yolk ; me.s. mesoblastic somite ; ao. aorta.
is converted into the muscles, both of the limbs and trunk, the superficial connective tissue, nervous sheath, etc. It probably also gives rise to the three muscles attached to the suctorial apparatus of the oesophagus.
The heart and aorta are formed as a solid rod of cells of the dorsal mesoblast, before it is distinctly divided into splanchnic and somatic layers. Eventually the central cells of the heart become blood corpuscles, while its walls are constituted of an outer muscular and inner epithelioid layer. It becomes functional, and acquires its valves, arterial branches, etc., by the stage represented in fig. 201 B.
The history of the mesoblast, more especially of the mesoblastic somites, of the Scorpion is very similar to that in Spiders : their cavity is continued in the same way into the limbs. The general character of the somites in the tail is shewn in fig. 207. The caudal aorta is stated by MetschnikofT to be formed from part of the mesenteron, but this is too improbable to be accepted without further confirmation.
The hypoblast and alimentary tract. It has already been stated that the yolk is to be regarded as corresponding to the hypoblast of other types.
For a considerable period it is composed of the polygonal yolk cells already described and shewn in figs. 203, 204, and 205. The yolk cells divide and become somewhat smaller as development proceeds ; but the main products of the division of the yolk nuclei and the protoplasm around them are undoubtedly cells which join the mesoblast (fig. 203 A). The permanent alimentary tract is formed of three sections, viz. stomodaeum, proctodaeum, and mesenteron. The stomodaeum and proctodaeum are both formed before the mesenteron. The stomodaeum is formed as an epiblastic pit between the two procephalic lobes (figs. 200 and 205, st). It becomes deeper, and by the latest stage figured is a deep pit lined by a cuticle and ending blindly. To its hinder section, which forms the suctorial apparatus of the adult, three powerful muscles (a dorsal and two lateral) are attached.
The proctodaeum is formed considerably later than the stomodaeum. It is a comparatively shallow involution, which forms the rectum of the adult. It is dilated at its extremity, and two Malpighian vessels early grow out from it.
The mesenteron is formed in the interior of the yolk. Its walls are derived from the cellular elements of the yolk, and the first section to be formed is the hinder extremity, which appears as a short tube ending blindly behind in contact with the proctodaeum, and open to the yolk in front. The later history of the mesenteron has not been followed, but it undoubtedly includes
FlG. 207. TAIL OF AN ADVANCED EMBRYO OF THE SCORPION TO ILLUSTRATE THE STRUCTURE OF THE MESOBLASTIC
SOMITES. (After Metschnikoff.)
al. alimentary tract; an.i. anal invagination ; ep. epiblast ; me.s. mesoblastic somite.
the whole of the abdominal section of the alimentary canal of the adult, except the rectum, and probably also the thoracic section. The later history of the yolk which encloses the mesenteron has not been satisfactorily studied, though it no doubt gives rise to the hepatic tubes, and probably also to the thoracic diverticula of the alimentary tract.
The general history of the alimentary tract in Scorpio is much the same as in Spiders. The hypoblast, the origin of which as mentioned above is somewhat uncertain, first appears on the ventral side and gradually spreads so as to envelop the yolk, and form the wall of the mesenteron, from which the liver is formed as a pair of lateral outgrowths. The proctodaeum and stomodseum are both short, especially the former (vide fig. 207).
Summary and general conclusions.
The embryonic forms of Scorpio and Spiders are very similar, but in spite of the general similarity of Chelifer to Scorpio, the embryo of the former differs far more from that of Scorpio than the latter does from Spiders. This peculiarity is probably to be explained by the early period at which Chelifer is hatched ; and though a more thorough investigation of this interesting form is much to be desired, it does not seem probable that its larva is a primitive type.
The larvae of the Acarina with their peculiar ecdyses are to be regarded as much modified larval forms. It is not however easy to assign a meaning to the hexapodous stage through which they generally pass.
With reference to the segments and appendages, some interesting points are brought out by the embryological study of these forms.
The maximum number of segments is present in the Scorpion, in which nineteen segments (not including the praeoral lobes, but including the telson) are developed. Of these the first twelve segments have traces of appendages, but the appendages of the six last of these (unless the pecten is an appendage) atrophy. In Spiders there are indications in the embryo of sixteen segments ; and in all the Arachnida, except the Acarina, at the least four segments bear appendages in the embryo which are without them in the adult. The morphological bearings of this fact are obvious.
It deserves to be noted that, in both Scorpio and the Spider, the chelicerae are borne in the embryo by the first post-oral segment, and provided with a distinct ganglion, so that they cannot correspond (as they are usually supposed to do) with the antennae of Insects, which are always developed on the prae-oral lobes, and never supplied by an independent ganglion.
The chelicerae would seem probably to correspond with the mandibles of Insects, and the antennae to be absent. In favour of this view is the fact that the embryonic ganglion of the mandibles of Insects is stated (cf. Lepidoptera, Hatschek, p. 340) to become, like the ganglion of the chelicerae, converted into part of the cesophageal commissure.
If the above considerations are correct, the appendages of the Arachnida retain in many respects a very much more primitive condition than those of Insects. In the first place, both the chelicerae and pedipalpi are much less differentiated than the mandibles and first pair of maxillae with which they correspond. In the second place, the first pair of ambulatory limbs must be equivalent to the second pair of maxillae of Insects, which, for reasons stated above, were probably originally ambulatory. It seems in fact a necessary deduction from the arguments stated that the ancestors of the present Insecta and Arachnida must have diverged from a common stem of the Tracheata at a time when the second pair of maxillae were still ambulatory in function.
With reference to the order of the development of the appendages and segments, very considerable differences are noticeable in the different Arachnoid types. This fact alone appears to me to be sufficient to prove that the order of appearance of the appendages is often a matter of embryonic convenience, without any deep morphological significance. In Scorpio the segments develop successively, except perhaps the first postoral, which is developed after some of the succeeded segments have been formed. In Spiders the segment of the chelicerae, and probably also of the pedipalpi, appears later than the next three or four. In both these types the segments arise before the appendages, but the reverse appears to be the case in Chelifer. The permanent appendages, except the chelicerae, appear simultaneously in Scorpions and Spiders. The second pair appears long before the others in Chelifer, then the third, next the first, and finally the three hindermost.
(434) El. Metschnikoff. " Embryologie des Scorpions." Zeit.f.wiss. Zool. Bd. xxi. 1870.
(435) H. Rathke. Reisebemerkungen aus Taurien (Scorpio), Leipzig, 1837.
(436) El. Metschnikoff. " Entwicklungsgeschichte d. Chelifer." Zeit.f.wiss. Zool., Bd. xxi. 1870.
(437) A. Stecker. " Entwicklung der Chthonius-Eier im Mutterleibe und die Bildung des Blastoderms." Sitzung. konigl. bohmisch. Gesellschaft Wissensch., 1876, 3. Heft, and Aimed, and Mag. Nat. History, 1876, xvm. 197.
(438) M. Balbiani. " Memoire sur le developpement des Phalangides." Ann. Scien. Nat. Series v. Vol. xvi. 1872.
(439) M. Balbiani. "Memoire sur le developpement des Araneides." Ann. Scien. Nat. Series v. Vol. xvn. 1873.
(440) F. M. Balfour. "Notes on the development of the Araneina." Quart. Journ. of Micr. Science, Vol. xx. 1880.
(441) J. Barrois. " Recherches s. 1. developpement des Araigndes. " Journal de 1'Anat. et de la Physiol. 1878.
(442) E. Claparede. Recherches s. t evolution des Araignees. Utrecht, 1862.
(443) Hero Id. De generatione Araneorum in Ovo. Marburg, 1824.
(444) H. Ludwig. "Ueber die Bildung des Blastoderms bei den Spinnen." Zeit.f. wiss. Zool., Vol. xxvi. 1876.
(445) P. van Beneden. " Developpement de 1'Atax ypsilophora." Acad. Bruxelles, t. xxiv.
(446) Ed. Claparede. "Studien iiber Acarinen." Zeit.f. wiss. Zool., Bd. xvm. 1868.
Formation of the layers and the embryonic envelopes in the
There is a striking constancy in the mode of formation of the layers throughout the group. In the first place the hypoblast is not formed by a process which can be reduced to invagination : in other words, there is no gastrula stage.
Efforts have been made to shew that the mesoblastic groove of Insects implies a modified gastrula, but since it is the essence of a gastrula that it should directly or indirectly give rise to the archenteron, the groove in question cannot fall under this category. Although the mesoblastic groove of Insects is not a gastrula, it is quite possible that it is the rudiment of a blastopore, the gastrula corresponding to which has now vanished from the development. It would thus be analogous to the primitive streak of Vertebrates 1 .
The growth of the blastoderm over the yolk in Scorpions admits no doubt of being regarded as an epibolic gastrula. The blastopore would however be situated dorsally, a position which it does not occupy in any gastrula type so far dealt with. This fact, coupled with the consideration that the partial segmentation of Scorpio can be derived without difficulty from the ordinary Arachnidan type (vide p. 120), seems to shew that there is no true epibolic invagination in the development of Scorpio.
On the formation of the blastoderm traces of two embryonic layers are established. The blastoderm itself is essentially the epiblast, while the central yolk is the hypoblast. The formation of the embryo commences in connection with a thickening of the blastoderm, known as the ventral plate. The mesoblast is formed as an unpaired plate split off from the epiblast of the ventral plate. This process takes place in at any rate two ways. In Insects a groove is formed, which becomes constricted off to form the mesoblastic plate : in Spiders there is a keel-like thickening of the blastoderm, which takes the place of the groove.
The unpaired mesoblastic plate becomes in all forms very soon divided into two mesoblastic bands.
The mesoblastic bands are very similar to, and probably homologous with, those of Chaetopoda ; but the different modes by which they arise in these two groups are very striking, and probably indicate that profound modifications have taken place in the early development of the Tracheata. In the Chaetopoda the bands are from the first widely separated, and gradually approach each other ventrally, though without meeting. In the Tracheata they arise from the division of an unpaired ventral plate.
The further history of the mesoblastic bands is nearly the
1 The primitive streak of Vertebrates, as will appear in the sequel, has no connection with the medullary groove, and is the rudiment of the blastopore.
same for all the Tracheata so far investigated, and is also very much the same as for the Chaetopoda. There is a division into somites; each containing a section of the body cavity. In the cephalic section of the mesoblastic bands a section of the body cavity is also formed. In Arachnida, Myriapoda, and probably also Insecta, the body cavity is primitively prolonged into the limbs.
In Spiders at any rate, and very probably in the other groups of the Tracheata, a large part of the mesoblast is not derived from the mesoblastic plate, but is secondarily added from the yolk-cells.
In all Tracheata the yolk-cells give rise to the mesenteron which, in opposition, as will hereafter appear, to the mesenteron of the Crustacea, forms the main section of the permanent alimentary tract.
One of the points which is still most obscure in connection with the embryology of the Tracheata is the origin of the embryonic membranes. Amongst Insects, with the exception of the Thysanura, such membranes are well developed. In the other groups definite membranes like those of Insects are never found, but in the Scorpion a cellular envelope appears to be formed round the embryo from the cells of the blastoderm, and more or less similar structures have been described in some Myriapods (vide p. 390). These structures no doubt further require investigation, but may provisionally be regarded as homologous with the amnion and serous membrane of Insects. In the present state of our knowledge it does not seem easy to give any explanation of the origin of these membranes, but they may be in some way derived from an early ecdysis.
CRUSTACEA 1 .
History of the larval forms 1 '.
THE larval forms of the Crustacea appear to have more faithfully preserved their primitive characters than those of almost any other group.
The Branchiopoda, comprising under that term the Phyllopoda and Cladocera, contain the Crustacea with the maximum number of segments and the least differentiation of the separate appendages. This and other considerations render it probable that they are to be regarded as the most central group of the Crustaceans, and as in many respects least modified from the ancestral type from which all the groups have originated.
1 The following is the classification of the Crustacea employed in the present chapter.
i Phyllopoda. ( Natantia.
I. Branchiopoda. ciadocenu III. Copepoda. Euc P e P da Iparasita.
( Branchiura T Nebaliadse. jThoracica.
M f Sat- < v - wdi, p a minai ia
II. Malacostraca. ] Stomatopoda . ULocephaia.
I Cumacese. v. Ostracoda.
2 The importance of the larval history of the Crustacea, coupled with our comparative ignorance of the formation of the layers, has rendered it necessary for me to diverge somewhat from the general plan of the work, and to defer the account of the formation of the layers till after that of the larval forms.
The free larval stages when such exist commence with a larval form known as the Nauplius.
The term Nauplius was applied by O. F. Muller to certain larval forms of the Copepoda (fig. 229) in the belief that they were adult.
The term has now been extended to a very large number of larvae which have certain definite characters in common. They are provided (fig. 208 A) with three pairs of appendages, the future two pairs of antennae and mandibles. The first pair of antennae (an 1 ) is uniramous and mainly sensory in function, the second pair of antennae (an*) and mandibles (md) are biramous
FlG. 208. TWO STAGES IN THE DEVELOPMENT OF APUS CANCRIFORM1S.
A. Nauplius stage at the time of hatching.
B. Stage after first ecdysis.
an 1 , and a 2 . First and second antennae ; md. mandible ; MX. maxilla ; /. labrum; fr. frontal sense organ ; /. caudal fork ; s. segments.
swimming appendages, and the mandibles are without the future cutting blade. The Nauplius mandibles represent in fact the palp. The two posterior appendages are both provided with hook-like prominences on their basal joints, used in mastication. The body in most cases is unsegmented, and bears anteriorly a single median eye. There is a large upper lip, and an alimentary canal formed of cesophagus, stomach and rectum. The anus opens near the hind end of the body. On the dorsal surface small folds of skin frequently represent the commencement of a dorsal shield. One very striking peculiarity of the Nauplius according to Claus and Dohrn is the fact that the second pair of antennae is innervated from a sub-oesophageal ganglion. A larval form with the above characters occurs with more or less frequency in all the Crustacean groups. In most instances it
does not exactly conform to the above type, and the divergences are more considerable in the Phyllopods than in most other groups. Its characters in each case are described in the sequel. Phyllopoda. For the Phyllopoda the development of Apus cancriformis may conveniently be taken as type (Claus, No. 454). The embryo at the time it leaves the egg (fig. 208 A) is somewhat oval in outline, and narrowed posteriorly. There is a slight V-shaped indentation behind, at the apex of which is situated the anus. The body, unlike that of the typical Nauplius, is already divided into two regions, a cephalic and post-cephalic. On the ventral side of the cephalic region there are present the three normal pairs of appendages. Foremost there are the small anterior antennae (an 1 ), which are simple unjointed rod-like bodies with two moveable hairs at their extremities. They are inserted at the sides of the large upperlip or labrum (/). Behind these are the posterior antennae, which are enormously developed and serve as the most important larval organs of locomotion. They are biramous, being formed of a basal portion with a strong hook-like bristle projecting from its inner side, an inner unjointed branch with three bristles, and an outer large imperfectly five-jointed branch with five long lateral bristles. The hook-like organ attached to this pair of appendages would seem to imply that it served in some ancestral form as jaws (Claus). This character is apparently universal in the embryos of true Phyllopods, and constantly occurs in the Copepoda, etc.
The third pair of appendages or mandibles (md) is attached close below the upper lip. They are as yet unprovided with cutting blades, and terminate in two short branches, the inner with two and the outer with three bristles.
At the front of the head there is the typical unpaired eye. On the dorsal surface there is already present a rudiment of the cephalic shield, continuous anteriorly with the labrum (/) or upper lip, the extraordinary size of which is characteristic of the larvae of Phyllopods. The post-cephalic region, which afterwards becomes the thorax and abdomen, contains underneath the skin rudiments of the five anterior thoracic segments and their appendages, and presents in this respect an important variation from the typical Nauplius form. After the first ecdysis the
larva (fig. 208 B) loses its oval form, mainly owing to the elongation of the hinder part of the body and the lateral extension of the cephalic shield, which moreover now completely covers over the head and has begun to grow backwards so as to cover over the thoracic region. At the second ecdysis there appears at its side a rudimentary shell gland. In the cephalic region two small papillae (fr) are now present at the front of the head close to the unpaired eye. They are of the nature of sense organs, and may be called the frontal sense papillae. They have been shewn by Claus to be of some phylogenetic importance. The three pairs of Nauplius appendages have not altered much, but a rudimentary cutting blade has grown out from the basal joint of the mandible. A gland opening at the base of the antennae is now present, which is probably equivalent to the green gland often present in the Malacostraca. Behind the mandibles a pair of simple processes has appeared, which forms the rudiment of the first pair of maxillae (mx).
In the thoracic region more segments have been added posteriorly, and the appendages of the three anterior segments are very distinctly formed. The tail is distinctly forked. The heart is formed at the second ecdysis, and then extends to the sixth thoracic segment : the posterior chambers are successively added from before backwards.
At the successive ecdyses which the larva undergoes new segments continue to be formed at the posterior end of the body, and limbs arise on the segments already formed. These limbs probably represent the primitive form of an important type of Crustacean appendage, which is of value for interpreting the parts of the various malacostracan appendages. They consist (fig. 209) of a basal portion (protopodite of Huxley) bearing two rami. The basal portion has two projections on the inner side. To the outer side of the basal portion there is attached a dorsally directed branchial sack (br) (epipodite of Huxley). The outer ramus (ex) (exopodite of Huxley) is formed of a single plate with marginal setae. The inner one (en) (endopodite of Huxley) is four-jointed, and a process similar to those of the basal joint is given off from the inner side of the three proximal joints.
At the third ecdysis several new features appear in the cephalic region, which becomes more prominent in the succeeding
stages. In the first place the paired eyes are formed at each side
of and behind the unpaired eye, second ly the posterior pair of maxillae is
formed though it always remains very
rudimentary. The shell gland becomes
fully developed opening at the base of
the first pair of maxillae. The dorsal
shield gradually grows backwards till it
covers its full complement of segments.
After the fifth ecdysis the Nauplius FIG. 209. TYPICAL PHYL . , . , , LOPOD APPENDAGE. (Copied
appendages undergo a rapid atrophy. f rom ciaus.)
The second pair of antennae especially ex. exopodite ; en. endo becomes reduced in size, and the man
dibular palp the primitive Nauplius portion bearing the two proxir . ..... , mal projections is not sharply
portion of the mandible is contracted separated from the endopoto a mere rudiment, which eventually dite completely disappears, while the blade is correspondingly enlarged and also becomes toothed. The adult condition is only gradually attained after a very large number of successive changes of skin.
The chief point of interest in the above development is the fact of the primitive Nauplius form becoming gradually converted without any special metamorphosis into the adult condition 1 .
Branchipus like Apus is hatched as a somewhat modified Nauplius, which however differs from that of Apus in the hinder region of the body having no indications of segments. It goes through a very similar metamorphosis, but is at no period of its metamorphosis provided with a dorsal shield : the second pair of antennae does not abort, and in the male is provided with clasping organs, which are perhaps remnants of the embryonic hooks so characteristic of this pair of antennas.
The larva of Estheria when hatched has a Nauplius form, a large upper lip, caudal fork and single eye. There are two functional pairs of swimming appendages the second pair of antennae and mandibles. The first pair of antennae has not been detected, and a dorsal mantle to form the shell is not developed. At the first moult the anterior pair of antennae arises as small stump-like structures, and a small dorsal shield is also formed. Rudiments of six or seven pairs of appendages sprout
1 Nothing appears to be known with reference to the manner in which it comes about that more than one appendage is borne on each of the segments from the eleventh to the twentieth. An investigation of this point would be of some interest with reference to the meaning of segmentation
out in the usual way, and continue to increase in number at successive moults : the shell is rapidly developed. The chief point of interest in the development of this form is the close resemblance of the young larva to a typical adult Cladocera (Claus). This is shewn in the form of the shell, which has not reached its full anterior extension, the rudimentary anterior antennae, the large locomotor second pair of antennas, which differ however from the corresponding organs in the Cladocera in the presence of typical larval hooks. Even the abdomen resembles that of Daphnia. These features perhaps indicate that the Cladocera are to be derived from some Phyllopod form like Estheria by a process of retrogressive metamorphosis. The posterior antennas in the adult Estheria are large biramous appendages, and are used for swimming ; and though they have lost the embryonic hook, they still retain to a larger extent than in other Phyllopod families their Nauplius characteristics.
The Nauplius form of the Phyllopods is marked by several definite peculiarities. Its body is distinctly divided into a cephalic and post-cephalic region. The upper lip is extraordinarily large, relatively very much more so than at the later stages. The first pair of antennae is usually rudimentary and sometimes even absent ; while the second pair is exceptionally large, and would seem to be capable of functioning not only as a swimming organ, but even as a masticating organ. A dorsal shield is nearly or quite absent.
Cladocera. The probable derivation of the Cladocera from a form similar to Estheria has already been mentioned, and it might have been anticipated that the development would be similar to that of the Phyllopods. The development of the majority of the Cladocera takes place however in the egg, and the young when hatched closely resembles their parents, though in the egg they pass through a Nauplius stage (Dohrn). An exception to the general rule is however offered by the case of the winter eggs of Leptodora, one of the most primitive of the Cladoceran
families. The summer eggs after Sars.)
FIG. 709 A. NAUPLIUS LARVA OF LEPTODORA IIYAI.INA FROM wiNTKR EGG. (Copied from Bronn ;
develop without metamor
- /'. antenna of first pair; an*, antenna of
phosis, but Sars (No. 461) second pair; ntd. mandible;/ caudal fork.
has discovered that the larva leaves the winter eggs in the form of a Nauplius (fig. 209). This Nauplius closely resembles that of the Phyllopods. The body is elongated and in addition to normal Nauplius appendages is marked by six pairs of ridges the indications of the future feet. The anterior antennae are as usual small ; the second large and biramous, but the masticatory bristle characteristic of the Phyllopods is not present. The mandibles are without a cutting blade. A large upper lip and unpaired eye are present.
The adult form is attained in the same manner as amongst the Phyllopods after the third moult.
Owing to the size and importance of the various forms included in the Malacostraca, greater attention has been paid to their embryology than to that of any other division of the Crustacea ; and the proper interpretation of their larval forms involves some of the most interesting problems in the whole range of Embryology.
The majority of Malacostraca pass through a more or less complicated metamorphosis, though in the Nebaliadae, the Cumaceae, some of the Schizopoda, a few Decapoda (Astacus, Gecarcinus, etc.), and in the Edriophthalmata, the larva on leaving the egg has nearly the form of the adult. In contradistinction to the lower groups of Crustacea the Nauplius form of larva is rare, though it occurs in the case of one of the Schizopods (Euphausia, fig. 212), in some of the lower forms of the Decapods (Penaeus, fig. 214), and perhaps also, though this has not been made out, in some of the Stomatopoda.
In the majority of the Decapoda the larva leaves the egg in a form known as the Zoaea (fig. 210). This larval form is characterised by the presence of a large cephalo thoracic t shield usually FIG. 210. ZO^EAOFTHIAPOLITA. (After'Claus.) , ., , , , , mxp*. second maxillipede.
armed with lateral, anterior, and dorsal spines. The caudal segments are well de B. II. 30
veloped, though wit/tout appendages, and the tail, which functions in swimming, is usually forked. The six posterior thoracic segments are, on the other hand, rudimentary or non-existent. There are seven anterior pairs of appendages shewn in detail in fig. 21 1, viz. the two pairs of antennae (At. I. and At. II.), neither of them used as swimming organs, the mandibles without a palp (ma 7 ), well-developed maxillae (two pairs, mx I and mx 2), and two or sometimes (Macrura) three pairs of biramous natatory maxillipeds (mxp I and mxp 2). Two lateral compound stalked eyes are present, together with a median Nauplius eye. The heart has in the majority of cases only one or two (Brachyura) pairs of ostia.
The Zoaea larva, though typically developed in the Decapoda, is not always present (e.g. Astacus and Homarus), and some
FIG. 211. THE APPENDAGES OF A CRAB Z<VEA.
.-//./. first antenna ; At. I I. second antenna ; md. mandible (without a palp); mx. \. first maxilla; mx. i. second maxilla; mxp. \. first maxilliped ; mxp. i. second maxilliped.
ex. exopodite ; en. endopodite.
times occurs in a very modified form. It makes its appearance in an altered garb in the ontogeny of some of the other groups.
The two Malacostracan forms, amongst those so far studied, in which the phylogenetic record is most fully preserved in the ontogeny, are Euphausia amongst the Schizopods and Penaeus amongst the Decapods.
Schizopoda. Euphausia leaves the egg (MetschnikofT, No. 4689) as a true Nauplius with only three pairs of appendages, the two hinder
biramous, and an unsegmented body. The second pair of antennae has not however the colossal dimensions so common in the lower types. A mouth is present, but the anus is undeveloped.
After the first moult three pairs of prominences the rudiments of the two maxillae and ist maxillipeds arise behind the Nauplius appendages (fig. 212). At the same time an anus appears between the two limbs of a rudimentary caudal fork ; and an unpaired eye and upper lip appear in front. After another moult (fig. 212) a lower lip is formed (UL) as a pair of prominences very similar to true appendages ; and a delicate cephalo-thoracic shield also becomes developed. Still later the cutting blade of the mandible is formed, and the palp (Nauplius appendage) is greatly
FIG. 212. NAUPLIUS OF EUPHAUSIA. (From Glaus; after Metschnikoff.) The Nauplius is represented shortly before an ecdysis, and in addition to the
proper appendages rudiments of the three following pairs are present.
OL. upper lip ; UL. lower lip ; Md. mandible ; MX', and MX", two pairs of
maxillae ; mf . maxilliped i .
reduced. The cephalo-thoracic shield grows over the front part of the embryo, and becomes characteristically toothed at its edge. There are also
two frontal papillae very similar to those already described in the Phyllopod larvae. Rudiments of the compound eyes make their appearance, and though no new appendages are added, those already present undergo further differentiations. They remain however very simple ; the maxillipeds especially are very short and resemble somewhat Phyllopod appendages.
Up to this stage the tail has remained rudimentary and short, but after a further ecdysis (Claus) it grows greatly in length. At the same time the cephalo-thoracic shield acquires a short spine directed backwards. The larva is now in a condition to which Claus has given the name of Protozoasa (fig. 213 A).
Very shortly afterwards the region immediately following the segments already formed becomes indistinctly segmented, while the tail is still without a trace of segmentation. The region of the thorax proper soon becomes distinctly divided into seven very short segments, while at the same time the now elongated caudal region has become divided into its normal number of segments (fig. 213 B). By this stage the larva has become
FIG. 213. LARVAE OF EUPHAUSIA. (After Claus.) From the side.
A. Protozorea larva. B. Zonea larva.
mx'. and tux", maxillre I and 2 ; mxp^. maxilliped r.
a true Zoaea though differing from the normal Zoaea in the fact that the thoracic region is segmented, and in the absence of a second pair of maxillipeds.
The adult characters are very gradually acquired in a series of successive moults ; the later development of Euphausia resembling in this respect that of the Phyllopods. On the other hand Euphausia differs from that group in the fact that the abdominal (caudal) and thoracic appendages develop as two independent series from before backwards, of which the abdominal series is the earliest to attain maturity.
This is shewn in the following table compiled from Claus' observations.
LENGTH OF LARVA.
APPENDAGES OF THORACIC REGION ; viz. the 2nd and 3rd maxilliped and 5 ambu latory appendages.
APPENDAGES OF ABDOMEN.
3 3^ mm.
2nd maxilliped, rudimentary.
ist abdominal appendage.
3 4 mm.
2nd maxilliped, biramous. 3rd rudimentary, ist and 2nd ambulatory appendages, rudimentary.
2nd and 3rd abdominal appendages. 4th and 5th rudimentary.
4^ 5 mm.
3rd maxilliped, biramous.
4 th, 5th, and 6th fully developed.
3rd and 4th ambulatory appendages.
5th ambulatory appendage.
All the appendages following the second pair of maxillas are biramous, and the first eight of these bear branched gills as their epipodites. It is remarkable that the epipodite is developed on all the appendages anteriorly in point of time to the outer ramus (exopodite).
Although in Mysis there is no free larval stage, and the development takes place in a maternal incubatory pouch, yet a stage may be detected which clearly corresponds with the Nauplius stage of Euphausia (E. van Beneden, No. 465). At this stage, in which only the three Nauplius appendages are developed, the Mysis embryo is hatched. An ecdysis takes place, but the Nauplius skin is not completely thrown off, and remains as an envelope surrounding the larva during its later development.
Decapoda. Amongst the Decapoda the larva usually leaves the egg in the Zoaea form, but a remarkable exception to this general rule is afforded by the case of one or more species of Penseus. Fritz M tiller was the first to shew that the larva of these forms leaves the egg as a typical Nauplius, and it is probable that in the successive larval stages of these forms the ancestral history of the Decapoda is most fully preserved 1 .
The youngest known larva of Penaeus (fig. 214) has a somewhat oval unsegmented body. There spring from it the three typical pairs of Nauplius appendages. The first is uniramous, the second and third are biramous, and both of them adapted
1 The doubts which have been thrown upon Miiller's observations appear to be quite unfounded.
for swimming, and the third of them (mandibles) is without a trace of the future blade. The body has no carapace, and bears anteriorly a single median simple eye. Posteriorly it is produced into two bristles.
After the first moult the larva has a rudiment of a forked tail, while a dorsal fold of skin indicates the commencement of
FIG. 214. NAUPLIUS STAGE OF PEN^EUS. (After Fritz Miiller.)
the cephalo-thoracic shield. A large provisional helmet-shaped upper lip like that in Phyllopods has also appeared. Behind the appendages already formed there are stump-like rudiments of the four succeeding pairs (two pairs of maxillae and two pairs of maxillipeds) ; and in a slightly older larva the formation of the mandibular blade has commenced, together with the atrophy of the palp or Nauplius appendage.
Between this and the next observed stage there is possibly a slight lacuna. The next stage (fig. 215) at any rate represents the commencement of the Zoaea series. The cephalo-thoracic shield has greatly grown, and eventually acquires the usual dorsal spine. The posterior region of the body is prolonged into a tail, which is quite as long as the whole of the remainder of the body. The four appendages which were quite functionless at the last stage have now sprouted into full activity. The
region immediately behind them is divided (fig. 215) into six segments (the six thoracic segments) without appendages, while somewhat later the five anterior abdominal segments become indicated, but are equally with the thoracic segments without feet. The mode of appearance of these segments shews that the thoracic and abdominal segments develop in regular succession from before backwards (Claus). Of the palp of the mandibles, as is usual amongst Zosea forms, not a trace remains, though in the youngest Zoaea caught by Fritz Miiller a very small rudiment of the palp was present. The first pair of antennae is unusually long, and the second pair continues to function as a biramous swimming organ ; the outer ramus is multiarticulate. The other appendages are fully jointed, and the two maxillipeds biramous. On the dorsal surface of the body the unpaired eye is still present, but on each side of it traces of the stalked eyes have appeared. Frontal sense organs like those of Phyllopods are also present.
From the Protozoaea form the larva passes into that of a true Zoaea with the usual appendages and spines, characterised however by certain remarkable peculiarities. Of these the most important are (i) the large size of the two pairs of antennae and the retention of its Nauplius function by the second of them ; (2) the fact that the appendages of the six thoracic segments appear as small biramous Schizopod legs, while the abdominal appendages, with the exception of the sixth, are still without
PROTOZO^EA STAGE OF PEN/EUS. (After Fritz Miiller.)
their swimming feet. The early appearance of the appendages of the sixth abdominal segment is probably correlated with their natatory function in connection with the tail. As a point of smaller importance which may be mentioned is the fact that both pairs of maxillae are provided with small respiratory plates (exopodites) for regulating the flow of water under the dorsal shield. From the Zoaea form the larva passes into a Mysis or Schizopod stage (fig. 216), characterised by the thoracic feet and maxillipeds resembling in form and function the biramous feet of Mysis, the outer ramus being at first in many cases much larger than the inner. The gill pouches appear at the base of these feet nearly at the same time as the endopodites become functional. At the same time the antennae become profoundly modified. The anterior antennae shed their long hairs, and from the inner side of the fourth joint there springs a new process,
FIG. 216. PEN^EUS LARVA IN THE MYSIS STAGE. (After Claus.)
which eventually elongates and becomes the inner flagellum. The outer ramus of the posterior antennae is reduced to a scale, while the flagellum is developed from a stump-like rudiment of the inner ramus (Claus). A palp sprouts on the mandible and the median eye disappears.
The abdominal feet do not appear till the commencement of the Mysis stage, and hardly become functional till its close.
From the Mysis stage the larva passes quite simply into the adult form. The outer ramus of the thoracic feet is more or less completely lost. The maxillipeds, or the two anterior pairs at any rate, lose their ambulatory function, cutting plates develop on the inner side of their basal joints, and the two rami persist
as small appendages on their outer side. Gill pouches also sprout from their outer side.
The respiratory plate of the second maxilla attains its full development and that on the first maxilla disappears 1 . The Nauplius, so far as is known, does not occur in any other Decapod form except Penaeus.
The next most primitive larval history known is that which appears in the Sergestidae. The larval history, which has been fully elucidated by Claus, commences with a Protozoaea form (fig. 217), which develops into a remarkable Zoaea first described by Dohrn as Elaphocaris. This develops into a form originally described by Claus as Acanthosoma, and this into a form known as Mastigopus (fig. 218) from which it is easy to pass to the adult.
The remarkable Protozoaea (fig. 217) is characterised by the presence on the dorsal shield of a frontal, dorsal and two lateral spikes, each richly armed with long side spines. The
FIG. 217. LATEST PROTOZO^A STAGE OF SEK GESTES LARVA (ELAPHOCARIS). (After Claus.)
mxp'" '. third pair of maxillipeds.
normal Zoasa appendages are present, and in addition to them a small third pair of maxillipeds. The thoracic region is divided into five short rings, but the abdomen is unsegmented. The tail is forked and provided with long spines. The antennae, like those of Penasus, are long the second pair biramous ; the mandibles unpalped. Both pairs of maxillae are provided with respiratory plates ; the second pair is footlike, and has at its base a glandular mass believed by Claus to be the equivalent of the Entomostracan shell-gland. The maxillipeds have the usual biramous characters. A
1 From Claus' observations (No. 448) it would appear that the respiratory plate is only the exopodite and not, as is usually stated, the coalesced exopodite and epipodite. Huxley in his Comparative Anatomy reserves this point for embryological elucidation.
FIG. 218. MASTIGOPUS STAGE OF SERGESTES. (From Claus.) Mf". maxilliped 3.
helmet-shaped upper lip like that of a typical Nauplius is present, and the eyes are situated on very long stalks.
In the true Zoaea stage there appear on the five thoracic
segments pouch-like biramous rudiments of the limbs. The tail becomes segmented; but the segments, with the exception of the sixth, remain without appendages. On the sixth a very long bilobed pouch appears as the commencement of the swimming feet of this segment. The segments of the abdomen are armed with lateral spines.
From the Zoaea stage the larva passes into the form known as Acanthosoma, which represents the Mysis stage of Penaeus. The complex spikes on the dorsal shield of the Zoaea stage are reduced to simple spines, but the spines of the tail still retain their full size. In the appendages the chief changes consist (i) in the reduction of the jointed outer ramus of the second pair of antennae to a stump representing the scale, and the elongation of the inner one to the flagellum ; (2) in the elongation of the five ambulatory thoracic appendages into biramous feet, like the maxillipeds, and in the sprouting forth of rudimentary abdominal feet.
The most obvious external indications of the passage from the Acanthosoma to the Mastigopus stage (fig. 218) are to be found in the elongation of the abdomen, the reduction and flattening of the cephalo-thoracic shield, and the nearly complete obliteration of all the spines but the anterior. The eyes on their elongated stalks are still very characteristic, and the elongation of the flagellum of the second pair of antennae is very striking.
The maxillae and maxillipeds undergo considerable metamorphosis, the abdominal feet attain their adult form, and the three anterior thoracic ambulatory legs lose their outer rami. The most remarkable change of all concerns the two last pairs of thoracic appendages, which, instead of being metamorphosed like the preceding ones, are completely or nearly completely thrown off in the moult which inaugurates the Mastigopus stage, and are subsequently redeveloped. With the reappearance of these appendages, and the changes in the other appendages already indicated, the adult form is practically attained.
FIG. 219. LARVA OF HIPPOLYTE IN ZO/EA STAGE. (From Claus.)
MX', and MX", maxillae i and 2 ; Mf. Mf. Mf". maxillipeds.
OLDER LARVA OF HIPPOLYTE AFTER THE THORACIC APPENDAGES HAVE BECOME FORMED. (From Claus.)
With reference to the development of the majority of the Carabidae, Penaeinae, Palaemoninae, Crangoninae, it may be stated generally that they leave the egg in the Zoaea stage (fig. 219) with anterior appendages up to the third pair of maxillipeds. The thorax is unsegmented and indeed almost unrepresented, but the abdomen is long and divided into distinct segments. Both thoracic and abdominal appendages are absent, and the tail is formed by a simple plate with numerous bristles, not forked, as in the case of the Zoaea of Fritz M tiller's Penaeus and Sergestes. A dorsal spine is frequently found on the second abdominal segment. From the Zoaea form the embryo passes into a Mysis stage (fig. 220), during which the thoracic appendages gradually appear as biramous swimming feet; they
FIG. 221. NEWLY-HATCHED LARVA OF THE AMERICAN LOBSTER. (After Smith.) are all developed before any of the abdominal appendages, except the last. In some cases the development is still further abbreviated. Thus the larvae of Crangon and Palaemonetes (Faxon, No. 476) possess at hatching the rudiments of the two anterior pairs of thoracic feet, and Palaemon of three pairs'.
Amongst the other Macrura the larva generally leaves the egg as a Zoaea similar to that of the prawns. In the case of the
1 Fritz Miiller has recently (Zoologisrher Anzeiger^ No. 52) described a still more abbreviated development of a Pala-mon living in brooks near Blumenau.
Thalassinidae and Paguridae a Mysis stage has disappeared. The most remarkable abbreviations of the typical development are presented on the one hand by Homarus and Astacus, and on the other by the Loricata.
The development of Homarus has been fully worked out by S. J. Smith (No. 491) for the American lobster (Homarus americanus). The larva (fig. 221) leaves the egg in an advanced Mysis stage. The cephalo-thoracic shield is fully developed, and armed with a rostrum in front. The first pair of antennae is unjointed but the second is biramous, the outer ramus forming a large Mysis-like scale. The mandibles, which are palped, the maxillae, and the two anterior maxillipeds differ only in minor details from the same appendages of the adult. The third pair of maxillipeds is Mysis-like and biramous, and the five ambulatory legs closely resemble them, the endopodite of the first being imperfectly chelate. The abdomen is well developed but without appendages. The second, third, fourth and fifth segments are armed with dorsal and lateral spines.
In the next stage swimming feet have appeared on the second, third, fourth and fifth abdominal segments, and the appendages already present have approached their adult form. Still later, when the larva is about half an inch in length, the approach to the adult form is more marked, and the exopodites of the ambulatory legs though present are relatively much reduced in size. The swimmerets of the sixth abdominal segment are formed. In the next stage observed the larva has entirely lost its Schizopod characters, and though still retaining its free swimming habits differs from the adult form only in generic characters.
As has been already stated, no free larval stages occur in the development of Astacus, but the young is hatched in a form in which it differs only in unimportant details from the adult.
The peculiar larval form of the Loricata (Scyllarus, Palinurus) has long been known under the name Phyllosoma (fig. 222 C), but its true nature was first shewn by Couch (No. 474) [Couch did not however recognise the identity of his larva with Phyllosoma ; this was first done by Gerstacker] and shortly afterwards by Gerbe and Coste. These observations were however for a long time not generally accepted, till Dohrn (No. 477) published his valuable memoir giving an account of how he succeeded in actually rearing Phyllosoma from the eggs of Scyllarus and Palinurus, and shewing that some of the most remarkable features of the metamorphosis of the Loricata occur before the larva is hatched.
The embryo of Scyllarus in the egg first of all passes through the usual Nauplius stage, and then after the formation of a cuticle develops an elongated thoracico-abdominal region bent completely over the anterior part of the body. There appear moreover a number of appendages and the rudiments of various organs ; and the embryo passes into a form which may be described as the embryonic Phyllosoma stage. In this stage there are present on the anterior part of the body, in front of the ventral flexure, two
pairs of antennae, mandibles, two pairs of maxillae, the second commencing to be biramous, and a small stump representing the first pair of maxillipeds. The part of the body bent over consists of a small quadrate caudal plate, and an appendage-bearing region to which are attached anteriorly three pairs of biramous appendages the second and third maxillipeds, and the anterior pair of ambulatory legs and two pairs of undivided appendages the second and third pairs of ambulatory legs. In a slightly later stage the first pair of maxillae becomes biramous, as also does the first pair of maxillipeds in a very rudimentary fashion. The second and third pairs of ambulatory legs become biramous, while the second and third maxilliped nearly completely lose their outer ramus. Very small rudiments of the two hinder ambulatory legs become formed. If the embryo is taken at this stage (vide fig. 222 A, which represents a nearly similar larva of Palinurus) out of the egg, it is seen to consist of (i) an anterior enlargement with a vaulted dorsal shield enclosing the yolk, two stalked eyes, and a median eye ; (2) a thoracic region in which the indications of segmentation are visible with the two
FIG. 222. LARWE OF THE LORICATA. (After Claus.)
A. Embryo of Palinurus shortly before hatching.
B. Young Phyllosoma larva of Scyllarus, without the first maxilliped, the two last thoracic appendages, or the abdominal appendages.
C. Fully-grown Phyllosoma with all the Decapod appendages.
at*, antenna of first pair ; at*, antenna of second pair ; md. mandible ; ntx 1 . first maxilla; mx 1 . second maxilla; mx^mxf. maxillipeds; / 1 / 3 . thoracic appendages.
posterior pairs of maxillipeds (mxfp and wr/ 3 ) and the ambulatory legs (/ l ); (3) an abdominal region distinctly divided into segments and ending in a fork. Before the embryo becomes hatched the first pair of maxillipeds becomes reduced in size and finally vanishes. The second pair of maxillae becomes reduced to simple stumps with a few bristles, the second pair of antennae
also appears to undergo a retrogressive change, while the two last thoracic segments cease to be distinguishable. It thus appears that during embryonic life the second pair of antennae, the second pair of maxillae, and the second and third pair of maxillipeds and the two hinder ambulatory appendages undergo retrogressive changes, while the first pair of maxillipeds is completely obliterated !
The general form of the larva when hatched (fig. 222 B) is not very different from that which it has during the later stages within the egg. The body is divided into three regions: (i) an anterior cephalic; (2) a middle thoracic, and (3) a small posterior abdominal portion ; and all of them are characterised by their extreme dorso-ventral compression, so that the whole animal has the form of a three-lobed disc, the strange appearance of which is much increased by its glass-like transparency.
The cephalic portion is oval and projects slightly behind so as to overlap the thorax. Its upper surface constitutes the dorsal shield, from which there spring anteriorly the two compound eyes on long stalks, between which is a median Nauplius eye. The mouth is situated about the middle of the under surface of the anterior disc. It leads into a stomach from which an anterior and a lateral hepatic diverticulum springs out on each side. The former remains as a simple diverticulum through larval life, but the latter becomes an extremely complicated glandular structure.
At the front border of the disc is placed the unjointed but elongated first pair of antennae (rt/ 1 ). Externally to and behind these there spring the short posterior antennae (at'*}. At the base of which the green gland is already formed. Surrounding the mouth are the mandibles (md) and anterior pair of maxillae (mx 1 ), and some distance behind the second pair of maxillae (mx*), consisting of a cylindrical basal joint and short terminal joint armed with bristles. The first pair of maxillipeds is absent.
The thoracic region is formed of an oval segmented disc attached to the under surface of the cephalic disc. From its front segment arises the second pair of maxillipeds (inxp l } as single five-jointed appendages, and from the next segment springs the five-jointed elongated but uniramous third pair of maxillipeds (mxfl 3 }, and behind this there arise three pairs of six-jointed ambulatory appendages (p\ / 2 , p 3 , of which only the basal joint is represented in the figure) with an exopodite springing from their second joint. The two posterior thoracic rings and their appendages cannot be made out.
The abdomen is reduced to a short imperfectly segmented stump, ending in a fork, between the prongs of which the anus opens. Even the youngest larval Phyllosoma, such as has just been described, cannot be compared with a Zoaea, but belongs rather, in the possession of biramous thoracic feet, to a Mysis stage. In the forked tail and Nauplius eye there appear however to be certain very primitive characters carried on to this stage.
The passage of this young larva to the fully formed Phyllosoma (fig. 222 C) is very simple. It consists essentially in the fresh development of the first pair of maxillipeds and the two last ambulatory appendages, the growth and segmentation of the abdomen, and the sprouting on it of biramous
swimming feet. In the course of these changes the larva becomes a true Decapod in the arrangement and number of its appendages ; and indeed it was united with this group before its larval character was made out. In addition to the appearance of new appendages certain changes take place in those already present. The two posterior maxillipeds, in the Palinurus Phyllosoma at any rate, acquire again an exopodite, and together with the biramous ambulatory feet develop epipodites in the form of gill pouches.
The mode of passage of the Phyllosoma to the adult is not known, but it can easily be seen from the oldest Phyllosoma forms that the dorsal cephalic plate grows over the thorax, and gives rise to the cephalo-thoracic shield of the adult.
There are slight structural differences, especially in the antennae, between the Phyllosoma of Scyllarus and that of Palinurus, but the chief difference in development is that the first pair of maxillipeds of the Palinurus embryo, though reduced in the embryonic state, does not completely vanish, at any rate till after the free larval state has commenced ; and it is doubtful if it does so even then. The freshly hatched Palinurus Phyllosoma is very considerably more developed than that of Scyllarus.
Brachyura. All the Brachyura, with the exception of one or more species of land crabs 1 , leave the egg in the Zoaia condition, and though there are slight variations of structure, yet on the
FIG. 223. THE APPENDAGES OF A CRAB ZOJEA.
At. I. first antenna ; At. //. second antenna ; md. mandible (without a palp) ; mx. i. first maxilla ; mx. i. second maxilla ; w.r. 3. third maxilla ; mxp. i. first maxilliped ; mxp. i. second maxilliped.
ex. exopodite ; ett. cndopodite.
whole the Crab Zoaea is a very well marked form. Immediately after leaving the egg (fig. 210) it has a somewhat oval shape
1 It has been clearly demonstrated that the majority of land-crabs leave the egg in the 7.oxa. form.
with a long distinctly-segmented abdomen bent underneath the thorax. The cephalo-thoracic shield covers over the front part of the body, and is prolonged into a long frontal spine pointing forwards, and springing from the region between the two eyes ; a long dorsal spine pointing backwards ; and two lateral spines.
To the under surface of the body are attached the anterior appendages up to the second maxilliped, while the six following pairs of thoracic appendages are either absent or represented only in a very rudimentary form. The abdomen is without appendages.
The anterior antennae are single and unjointed, but provided at their extremity with a few olfactory hairs (only two in Carcinus Mcenas) and one or two bristles. The rudiment of the secondary flageltum appears in very young Zoaeae on the inner side of the antennules (fig. 223 At. /.). The posterior antennae are without the flagellum, but are provided with a scale representing the exopodite (fig. 223 At. II. ex] and usually a spinous
FIG. 224. CRAB ZO^EA AFTER TH.. THIRD PAIR OF MAXILLIPEDS AND THE
THORACIC AND ABDOMINAL APPENDAGES HAVE BECOME DEVELOPED.
at 1 , antenna of first pair ; at z . antenna of second pair ; mx l . first maxilla ; mop. second maxilla ; mxp 1 . first maxilliped ; mxjP. second maxilliped ; mxf. third maxilliped ; oc. eye ; ht. heart.
process. The flagellum is very early developed and is represented in fig. 223, At. II. en. The mandibles (md) are large but without a palp. The anterior maxillae (mx i) have a short twojointed endopodite (palp) with a few hairs, and a basal portion B. II. 31
with two blades, of which the distal is the largest, both armed with stiff bristles. The posterior maxillae have a small respiratory plate (exopodite), an endopodite (palp) shaped like a double blade, and two basal joints each continued into a double blade. The two maxillipeds (inxp i and mxp 2) have the form and function of biramous swimming feet. The exopodite of both is two-jointed and bears long bristles at its extremity ; the endopodite of the anterior is five-jointed and long, that of the second is three-jointed and comparatively short.
In the six-jointed tail the second segment has usually two dorsally directed spines, and the three succeeding segments each of them two posteriorly directed. The telson or swimming plate is not at first separated from the sixth segment ; on each side it is prolonged into two well-marked prongs ; and to each prong three bristles are usually attached (fig. 224). The heart (fig. 224 ht) lies under the dorsal spine and is prolonged into an anterior, posterior, and dorsal aorta. It has only two pairs of venous ostia.
During the Zoaea stage the larva rapidly grows in size, and undergoes considerable changes in its appendages which reach the full Decapod number (fig. 224). On both pairs of antennae a flagellum becomes developed and grows considerably in length. Before the close of the Zoaea condition a small and unjointed palp appears on the mandible. Behind the second maxilliped the third maxilliped (inxp*} early appears as a small biramous appendage, and the five ambulatory feet become distinctly formed as uniramous appendages the exopodites not being present. The third pair of maxillipeds and three following ambulatory appendages develop gill pouches. The abdominal feet are formed on the second to the sixth segments of the tail as simple pouches.
The oldest Zoaea is transmuted at its moult into a form known as Megalopa, which is really almost identical with an anomurous Decapod. No Schizopod stage is intercalated, which shews that the development is in many respects greatly abbreviated. The essential characters of the Megalopa are to be found in (i) the reduction of the two anterior maxillipeds, which cease to function as swimming feet, and together with the appendages in front of them assume the adult form ; (2) the full
functional development of the five ambulatory appendages ; (3) the reduction of the forked telson to an oval swimming plate, and the growth in size of the abdominal feet, which become large swimming plates and are at the same time provided with short endopodites which serve to lock the feet of the two sides.
With these essential characters the form of the Megalopa differs considerably in different cases. In some instances (e.g. Carcinus mcenas) the Zoasa spines of the youngest Megalopa are so large that the larva appears almost more like a Zoasa than a Megalopa (Spence Bate, No. 470). In other cases, e.g. that represented on fig. 225, the Zoasa spines are still present but much reduced; and the cephalo-thoracic shield has very much the adult form. In other cases again (e.g. Portunus) the Zoasa spines are completely thrown off at the youngest Megalopa stage.
There is a gradual passage from the youngest Megalopa to the adult form by a series of moults.
Some of the brachyurous Zoasa forms exhibit considerable divergences from the described type, more espcially in the armature of the shield. In some forms the spines are altogether absent, e.g. Maja (Couch, No. 474) and Eurynome. In other forms the frontal spine may be much reduced or absent (Inachus and Achasus). The dorsal spine may also be absent, and in one form described by Dohrn (No. 478) there is a long frontal spine and two pairs of lateral spines, but no dorsal ^ MEGALOPA STAGE OF CRAB LARVA.
spine. Both dorsal and
frontal spines may attain enormous dimensions and be swollen at their extremities (Dohrn). A form has been described by Claus as Pterocaris in which the cephalo-thoracic shield is laterally expanded into two wing-like processes.
The Zoasa of Porcellana presents on the whole the most remarkable peculiarities and, as might be anticipated from the systematic position of the adult, is in some respects intermediate between the macrurous Zoasa and that of the Brachyura. It is characterized by the oval form of the body, and by
the presence of one enormously long frontal spine and two posterior spines. The usual dorsal spine is absent. The tail plate is rounded and has the character of the tail of a macrurous Zoaea, but in the young Zoasa the third pair of maxillipeds is absent and the appendages generally have a brachyurous character. A Megalopa stage is hardly represented, since the adult may almost be regarded as a permanent Megalopa.
Stomatopoda. The history of the larval forms of the Stomatopoda (Squilla etc.) has not unfortunately been thoroughly worked out, but what is known from the researches of Fritz Miiller (No. 495) and Claus (No. 494) is of very great importance. There are it appears two types, both of which used to be described as adult forms under the respective names Erichthus and Alima.
The youngest known Erichthus form is about two millimetres in length, and has the characters of a modified Zoaea (fig. 226). The body is divided into three regions, an anterior unsegmented region to which are attached two pairs of antennas, mandibles, and maxillae (two pairs). This portion has a dorsal shield covering the next or middle region, which consists of five segments each with a pair of biramous appendages. These appendages represent the five maxillipeds of the adult 1 . The portion of the body behind this is without appendages. It consists of three short anterior segments, the three posterior thoracic segments of the adult, and a long unsegmented tail. The three footless thoracic segments are covered by the dorsal shield. Both pairs of antennae are uniramous and comparatively short. The mandibles, like those of Phyllopods, are without palps, and the two following pairs of maxillae are small. The five maxillipeds have the characters of normal biramous Zoaea feet. From the front of the head spring a pair of compound eyes with short stalks, which grow longer in the succeeding stages ; between them is a median eye. The dorsal shield is attached just behind this eye, and is provided, as in the typical Zoaea, with a frontal spike while its hinder border is produced into two lateral spikes and one median. In a larva of about three millimetres a pair of biramous appendages arises behind the three footless thoracic segments. It is the anterior pair of abdominal feet (fig. 226). The inner ramus of the second pair of maxillipeds soon grows greatly in length, indicating its subsequent larger size and prehensile form (fig. 227 g). When the larva after one or
two moults attains a length FlG - 6 - SECOND STAGE OF ERICHTHUS of six millimetres Cfitr 227 1 LARVA OFSQUII.LA WITH FIVE MAXILLIPEDS AND
(tig. 227) THE FIRST PAIR OF ABDOMINAL APPENDAGES.
the abdomen has six segments (From Claus.)
1 These five maxillipeds correspond with the three maxillipeds and two anterior ambulatory appendages of the Decapoda.
(the sixth hardly differentiated), each with a pair of appendages (the two hindermost still rudimentary) which have become gradually developed from before backwards. The three hindermost thoracic segments are still without appendages.
Some changes of importance have occurred in the other parts. Both antennas have acquired a second flagellum, but the mandible is still without
FIG. 227. ADVANCED ERICHTHUS LARVA OF SQUILLA WITH FIVE PAIRS OF
ABDOMINAL APPENDAGES. (From Claus.)
f. first maxilliped ; g. second maxilliped.
a palp. The first and second pair of maxillipeds have both undergone important modifications. Their outer ramus (exopodite) has been thrown off, and a gill-plate (epipodite) has appeared as an outgrowth from their basal joint. Each of them is composed of six joints. The three following biramous appendages have retained their earlier characters but have become much reduced in size. In the subsequent moults the most remarkable new features concern the three posterior maxillipeds, which undergo atrophy, and are either completely lost or reduced to mere unjointed sacks (fig. 228). In
FIG. 228. ADVANCED ERICHTHUS LARVA OF SQUILLA WHEN THE THREE POSTERIOR MAXILLIPEDS HAVE BECOME REDUCED TO MINUTE POUCHES.
the stage where the complete Erichthus type has been reached, these three appendages have again sprouted forth in their permanent form and each of them is provided with a gill-sack on its coxal joint. Behind them the three ambulatory appendages of the thorax have also appeared, first as simple buds, which subsequently however become biramous. On their development the full number of adult appendages is acquired.
The most noteworthy points in the developmental history detailed above are the following :
(i) The thoracic and abdominal segments (apart from their appendages) develop successively from before backwards.
(2) The three last maxillipeds develop before the abdominal feet, as biramous appendages, but subsequently completely atrophy, and then sprout out again in their permanent form.
(3) The abdominal feet develop in succession from before backwards, and the whole series of them is fully formed before a trace of the appendages of the three hindermost thoracic segments has appeared. It may be mentioned as a point of some importance that the Zoaea of Squilla has an elongated many-chambered heart, and not the short compact heart usually found in the Zoaea.
The younger stages of the Alima larva are not known 1 , but the earliest stage observed is remarkable for presenting no trace of the three posterior pairs of maxillipeds, or of the three following pairs of thoracic appendages. The segments belonging to these appendages are however well developed. The tail has its full complement of segments with the normal number of well developed swimming feet. The larva represents in fact the stage of the Erichthus larva when the three posterior pairs of maxillipeds have undergone atrophy ; but it is probable that these appendages never become developed in this form of larva.
Apart from the above peculiarities the Alima form of larva closely resembles the Erichthus form.
Nebaliadae. The development of Nebalia is abbreviated, but from MetschnikofFs figures 2 may be seen to resemble closely that of Mysis. The abdomen has comparatively little yolk, and is bent over the ventral surface of the thorax. There is in the egg a Nauplius stage with three appendages, and subsequently a stage with the Zoaea appendages.
The larva when it leaves the egg has the majority of its appendages formed, but is still enveloped in a larval skin, and like Mysis bends its abdomen towards the dorsal side. When the larva is finally hatched it does not differ greatly from the adult.
Cum ace ae. The development of the Cumaceae takes place for the most part within the egg, and has been shewn by Dohrn (No. 496) to resemble in many points that of the Isopods. A dorsal organ is present, and a fold is formed immediately behind this which gives to the embryo a dorsal flexure. Both of these features are eminently characteristic of the Isopoda.
The formation of the two pairs of antennie, mandibles, and two pairs of maxillae and the following seven pairs of appendages takes place very early. The pair of appendages behind the second maxilku assumes an ambulatory form, and exhibits a Schizopod character very early, differing in both these respects from the homologous appendages in the Isopoda. The cephalo-thoracic shield commences to be formed when the appendages are still quite rudimentary as a pair of folds in the maxillary region. The
1 The observations of Brooks (No. 493) render it probable that the Alima larva leaves the egg in a form not very dissimilar to the youngest known larva. 3 His paper is unfortunately in Russian.
eyes are formed slightly later on each side of the head, and only coalesce at a subsequent period to form the peculiar median sessile eye of the adult.
The two pairs of appendages behind the second maxillae become converted into maxillipeds, and the exopodite of the first of them becomes the main ramus, while in the externally similar second maxilliped the exopodite atrophies and the endopodite alone remains.
The larva is hatched without the last pair of thoracic limbs or the abdominal appendages (which are never developed in the female), but in other respects closely resembles the adult. Before hatching the dorsal flexure is exchanged for a ventral one, and the larva acquires a character more like that of a Decapod.
Natantia. The free Copepoda are undoubtedly amongst the lowest forms of those Crustacea which are free or do not lead a parasitic existence. Although some features of their anatomy, such for instance as the frequent absence of a heart, may be put down to a retrogressive development, yet, from their retention of the median frontal eye of the Nauplius as the sole organ of vision 1 , their simple biramous swimming legs, and other characters, they may claim to be very primitive forms, which have diverged to no great extent from the main line of Crustacean development. They supply a long series of transitional steps from the Nauplius stage to the adult condition.
While still within the egg-shell the embryo is divided by two transverse constrictions into three segments, on which the three Nauplius appendages are developed, viz. the two pairs of antennae and the mandibles. When the embryo is hatched the indication of a division into segments has vanished, but the larva is in the fullest sense a typical Nauplius 2 . There are slight variations in the shape of the Nauplius in different genera, but its general form and character are very constant. It has (fig. 229 A) an oval unsegmented body with three pairs of appendages springing from the ventral surface. The anterior of these (at i) is uniramous, and usually formed of three joints which bear bristles on their under surface. The two posterior
1 The Pontellidse form an exception to this statement, in that they are provided with paired lateral eyes in addition to the median one.
2 The term Nauplius was applied to the larva of Cyclops and allied organisms by O. F. Muller under the impression that they were adult forms.
pairs of appendages are both biramous. The second pair of antennae (at 2) is the largest. Its basal portion (protopodite) bears on its inner side a powerful hook-like bristle. The outer ramus is the longest and many-jointed ; the inner ramus has only two joints. The mandibles (md), though smaller than the second pair of antennae, have a nearly identical structure. No blade-like projection is as yet developed on their protopodite. Between the points of insertion of the first pair of antennae is the median eye (oc), which originates by the coalescence of two distinct parts. The mouth is ventral, and placed in the middle line between the second pair of antennae and the mandibles : it
FIG. 229. SUCCESSIVE STAGES IN THE DEVELOPMENT OF CYCLOPS TENUICORMS.
(Copied from Bronn ; after Claus.)
A. B. and C. Nauplius stages. D. Youngest Copepod stage. In this figure maxillae and the two rami of the maxilliped are seen immediately behind the mandible md.
oc. eye ; at 1 , first pair of antennae ; a/ 8 , second pair of antennre ; md. mandible ; /*. first pair of feet ; / 2 . second pair of feet ; f. third pair of feet ; //. excretory concretions in the intestine.
is provided with an unpaired upper lip. There are two bristles at the hind end of the embryo between which the anus is placed, and in some cases there is at this part a slight indication of the future caudal fork.
The larva undergoes a number of successive ecdyses, at each of which the body becomes more elongated, and certain other
changes take place. First of all a pair of appendages arises behind the mandibles, which form the maxillae (fig. 229 B) ; at the same time the basal joint of the maxillae develops a cuttingblade. Three successive pairs of appendages (fig. 229 C) next become formed the so-called maxillipeds (the homologues of the second pair of maxillae), and the two first thoracic limbs. Each of these though very rudimentary is nevertheless bifid. The body becomes greatly elongated, and the caudal fork more developed.
Up to this stage of development the Nauplius appendages have retained their primitive character almost unaltered ; but after a few more ecdyses a sudden change takes place ; a cephalothoracic shield becomes fully developed, and the larva comes to resemble in character an adult Copepod, from which it mainly differs in the smaller number of segments and appendages. In the earliest 'Cyclops' stage the same number of appendages are present as in the last Nauplius stage. There (fig. 229 D) is a well developed cephalo-thorax, and four free segments behind it. To the cephalo-thoracic region the antennae, mandibles, maxillae, the now double pair of maxillipeds (derived from the original single pair of appendages), and first pair of thoracic appendages (p l ) are attached. The second pair of thoracic appendages (/ 2 ) is fixed to the first free segment, and the rudiment of a third pair (/ 3 ) projects from the second free segment. The first pair of antennae has grown longer by the addition of new joints, and continues to increase in length in the following ecdyses till it attains its full adult development, and then forms the chief organ of locomotion. The second pair of antennae is much reduced and has lost one of its rami. The two rami of the mandibles are reduced to a simple palp, while the blade has assumed its full importance. The maxillae and following appendages have greatly increased in size. They are all biramous, though the two rami are not as yet jointed. The adult state is gradually attained after a number of successive ecdyses, at which new segments and appendages are added, while new joints are formed for those already present.
Parasita. The earliest developmental stages of the parasitic types of Copepoda closely resemble those of the free forms, but, as might be expected from the peculiarly modified forms of the adult, they present a
large number of secondary characters. So far as is known a more or less modified Nauplius larva is usually preserved.
The development of Achtheres percarum, one of the Lernaeopoda parasitic in the mouth, etc. of the common Perch, may be selected to illustrate the mode of development of these forms. The larva leaves the egg as a much simplified Nauplius (fig. 230 A). It has an oval body with only the two anterior pairs of Nauplius appendages ; both of them in the rudimentary condition of unjointed rods. The usual median eye is present, and there is also found a peculiar sternal papilla, on which opens a spiral canal filled with a glutinous material, which is probably derived from a gland which disappears on the completion of the duct. The probable function of this
FIG. 330. SUCCESSIVE STAGES IN THE DEVELOPMENT OF ACHTHERES PERCARUM. (Copied from Bronn ; after Claus. )
A. Modified Nauplius stage. B. Cyclops stage. C. Late stage of male embryo. D. Sexually mature female. E. Sexually mature male.
at 1 , first pair of antennae; at 3 , second pair of antennae; tnd. mandible; tnx. maxillae ; ptn 1 . outer pair of maxillipeds ; ftn^. inner pair of maxillipeds ; J> 1 . first pair of legs ; /*. second pair of legs ; z. frontal organ ; i. intestine ; o. larval eye ; b. glandular body ; t. organ of touch ; ov. ovary ; /. rod projecting from coalesced maxillipeds ; g. cement gland ; rs. receptaculurn seminis ; n. nervous system ; te. testis ; v. vas deferens.
organ is to assist at a later period in the attachment of the parasite to its host. Underneath the Nauplius skin a number of appendages are visible, which become functional after the first ecdysis. This takes place within a few hours after the hatching of the Nauplius, and the larva then passes from
this rudimentary Nauplius stage into a stage corresponding with the Cyclops stage of the free forms (fig. 230 B). In the Cyclops stage the larva has an elongated body with a large cephalo-thoracic shield, and four free posterior segments, the last of which bears a forked tail.
There are now present eight pairs of appendages, viz. antennae (two pairs), mandibles, maxillae, maxillipeds, and three pairs of swimming feet. The Nauplius appendages are greatly modified. The first pair of antennae is three-jointed, and the second biramous. The outer ramus is the longest, and bears a claw-like bristle at its extremity. This pair of appendages is used by the larva for fixing itself. The mandibles are small and connected with the proboscidiform mouth ; and the single pair of maxillae is small and palped. The maxillipeds (pm* and flm 2 ) are believed by Claus to be primitively a single biramous appendage, but early appear as two distinct structures 1 , the outer and larger of which becomes the main organ by which the larva is fixed. Both are at this stage simple two-jointed appendages. The two anterior pairs of swimming feet have the typical structure, and consist of a protopodite bearing an unjointed exopodite and endopodite. The first pair is attached to the cephalo-thorax and the second (p*} to the first free thoracic segment. The third pair is very small and attached to the second free segment. The mouth is situated at the end of a kind of proboscis formed by prolongations of the upper and lower lips. The alimentary tract is fairly simple, and the anus opens between the caudal forks.
Between this and the next known stage it is quite possible that one or more may intervene. However this may be the larva in the next stage observed (fig. 230 C) has already become parasitic in the mouth of the Perch, and has acquired an elongated vermiform aspect. The body is divided into two sections, an anterior unsegmented, and a posterior formed of five segments, of which the foremost is the first thoracic segment which in the earlier stage was fused with the cephalo-thorax. The tail bears a rudimentary fork between the prongs of which the anus opens. The swimming feet have disappeared, so also has the eye and the spiral duct of the embryonic frontal organ. The outer of the two divisions of the maxilliped have undergone the most important modification, in that they have become united at their ends, where they form an organ from which an elongated rod (_/) projects, and attaches the larva to the mouth or gills of its host. The antennae and jaws have nearly acquired their adult form. The nervous system consists of supra- and infra-cesophageal ganglia and two lateral trunks given off from the latter. At this stage the males and females can already be distinguished, not only by certain differences in the rudimentary generative organs, but also by the fact that the outer branch of the maxillipeds is much longer in the female than in the male, and projects beyond the head.
In the next ecdysis the adult condition is reached. The outer maxilli 1 Van Beneden (No. 506) in the genera investigated by him finds that the two maxillipeds are really distinct pairs of appendages.
peds of the male (fig. 230 ,/>#*) separate again ; while in the female (fig. 230 D) they remain fused and develop a sucker. The male is only about one-fifth the length of the female. In both sexes the abdomen is much reduced.
In the genera Anchorella, Lernaeopoda, Brachiella and Hessia, Ed. van BenecUn (No. 506) has shewn that the embryo, although it passes through a crypto-Nauplius stage in the egg, is when hatched already in the Cyclops stage.
Branchiura. The peculiar parasite Argulus, the affinities of which with the Copepoda have been demonstrated by Claus (No. 511), is hatched in a Cyclops stage, and has no Nauplius stage. At the time of hatching it closely resembles the adult in general form. Its appendages are however very nearly those of a typical larval Copepod. The body is composed of a cephalo-thorax and free region behind this. The cephalo-thorax bears on its under surface antennae (two pairs), mandibles, maxillipeds, and the first pair of thoracic feet.
The first pair of antennae is three-jointed, but the basal joint bears a hook. The second pair is biramous, the inner ramus terminating in a hook. The mandible is palped, but the palp is completely separated from the cutting blade 1 . The maxilla would, according to Claus, appear to be absent.
The two typical divisions of the Copepod maxillipeds are present, viz. an outer and anterior larger division, and an inner and posterior smaller one. The first pair of thoracic feet, as is usual amongst Copepoda, is attached to the cephalo-thorax. It has not the typical biramous Copepod character. There are four free segments behind the cephalo-thorax, the last of which ends in a fork. Three of them bear appendages, which are rudimentary in this early larval stage. On the dorsal surface are present paired eyes as well as an unpaired median eye.
Between the larval condition and that of the adult a number of ecdyses intervene.
The larvae of all the Cirripedia, with one or two exceptions, leave the egg in the Nauplius condition. The Nauplii differ somewhat in the separate groups, and the post-nauplial stages vary not inconsiderably.
It will be most convenient to treat successively the larval
1 It seems not impossible that the appendage regarded by Claus as the mandibular palp may really represent the maxilla, which would otherwise seem to be absent. This mode of interpretation would bring the appendages of Argulus into a much closer agreement with those of the parasitic Copepoda. It does not seem incompatible with the existence of the stylet-like maxillse detected by Claus in the adult.
history of the four sub-orders, viz. Thoracica, Abdominalia, Apoda, and Rhizocephala.
Thoracica. The just hatched larvae at once leave the egg lamellae of their parent. They pass out through an opening in the mantle near the mouth, and during this passage the shell of the parent is opened and the movements of the cirriform feet cease.
The larval stages commence with a Nauplius 1 which, though regarded by Claus as closely resembling the Copepod Nauplius (figs. 231 and 232 A), certainly has very marked pecularities of its own, and in some respects approaches the Phyllopod Nauplius. It is in the youngest stage somewhat triangular in form, and covered on the dorsal side by a very delicate and hardly perceptible dorsal shield, which is prolonged laterally into two very peculiar conical horns (fig. 231 Ik), which are the most characteristic structures of the Cirriped Nauplius. They are connected with a glandular mass, the secretion from which passes out at their apex. Anteriorly the dorsal shield has the same extension as the body, but posteriorly it projects slightly.
An unpaired eye is situated on the ventral surface of the head, and immediately behind it there springs a more or less considerable upper lip (Ib), which resembles the Phyllopod labrum rather than that of the Copepoda. Both mouth and anus are present, and the hind end of the body is slightly forked in some forms, but ends in others, e.g. Lepas fascicularis, in an elongated spine. The anterior of the three pairs of Nauplius appendages (At*) is uniramous, and the two posterior (Af and md) are biramous. From the protopodites of both the latter spring strong hooks like those of the Copepod and Phyllopod Nauplii. In some Nauplii, e.g. that of Balanus, the appendages are at first not jointed, but in other Nauplii, e.g. that of Lepas fascicularis, the jointing is well marked. In Lepas fascicularis the earliest free Nauplius is enveloped in a larval skin, which is thrown off after a few hours. The Nauplii of all the Thoracica undergo a considerable number of moults before their appendages increase in number or segmentation of the body appears. During these moults they grow larger, and the posterior part of the
1 Alepas squalicola is stated by Koren and Danielssen to form an exception to this rule, and to leave the egg with six pairs of appendages.
body the future thoracic and abdominal region grows relatively in length. There also appear close to the sides of the unpaired eye two conical bodies, which correspond with the frontal sense organs of the Phyllopods. During their growth the different larvae undergo changes varying greatly in degree.
In Balanus the changes consist for the most part in the full segmentation of the appendages and the growth and distinctness
FIG. 231. NAUPLIUS LARVA OF LEPAS FASCICULARIS VIEWED FROM THE SIDE. oc. eye ; At. i. antenna of first pair ; At. 2. antenna of second pair ; md. mandible ; Ib. labrum ; an. anus; me. mesenteron; d.sp. dorsal spine; c.sp. caudal spine; Vp. ventral spine ; Ih. lateral horns.
of the dorsal shield, which forms a somewhat blunt triangular plate, broadest in front, with the anterior horns very long, and two short posterior spines. The tail also becomes produced into a long spine.
In Lepas fascicularis the changes in appearance of the Nauplius, owing to a great spinous development on its shield, are very considerable ; and, together with its enormous size, render it a very remarkable form. Dohrn (No. 520), who was the first to describe it, named it Archizoaea gigas.
The dorsal shield of the Nauplius of Lepas fascicularis (fig. 231) becomes somewhat hexagonal, and there springs from the middle of the dorsal surface an enormously long spine (d,sp], like the dorsal spine of a Zoa^a. The hind end of the shield is also produced into a long caudal spine (c.sfi] between which and the dorsal spine are some feather-like processes. From its edge there spring in addition to the primitive frontal horns three main pairs of horns, one pair anterior, one lateral, and one posterior, and smaller ones in addition. All these processes (with the exception of the dorsal and posterior spines) are hollow and open at their extremities, and like the primitive frontal horns contain the ducts of glands situated under the shield. On the under surface of the larva is situated the unpaired eye (pc] on each side of which spring the two-jointed frontal sense organs. Immediately behind these is the enormous upper lip (lb] which covers the mouth 1 . At the sides of the lip lie the three pairs of Nauplius appendages, which are very characteristic but present no special peculiarities. Posteriorly the body is produced into a long ventral spine-like process ( Vfi) homologous with that of other more normal Nauplii. At the base of this process large moveable paired spines appear at successive moults, six pairs being eventually formed. These spines give to the region in which they are situated a segmented appearance, and perhaps similar structures have given rise to the appearance of segmentation in Spence Bate's figures. The anus is situated on the dorsal side of this ventral process, and between it and the caudal spine of the shield above. The fact that the anus occupies this position appears to indicate that the ventral process is homologous with the caudal fork of the Copepoda, on the dorsal side of which the anus so often opens 2 .
From the Nauplius condition the larvae pass at a single moult into an entirely different condition known as the Cypris stage. In preparation for this condition there appear, during the last Nauplius moults, the rudiments of several fresh organs, which are more or less developed in different types. In the first place a compound eye is formed on each side of the median eye. Secondly there appears behind the mandibles a fourth pair of appendages the first pair of maxillae and internal to these a pair of small prominences, which are perhaps
1 Willemoes Suhm (No. 530) states that the mouth is situated at the free end of the upper lip, and that the oesophagus passes through it. From an examination of some specimens of this Nauplius, for which I am indebted to Moseley, I am inclined to think that this is a mistake, and that a groove on the surface of the upper lip has been taken by Suhm for the oesophagus.
2 The enormous spinous development of the larva of Lepas fascicularis is probably to be explained as a secondary protective adaptation, and has no genetic connection with the somewhat similar spinous armature of the Zosea.
equivalent to the second pair of maxillae, and give rise to the third pair of jaws in the adult (sometimes spoken of as the lower lip).
Behind these appendages there are moreover formed the rudiments of six pairs of feet. Under the cuticle of the first pair of antennae there may be seen just before the final moult the fourjointed antennae of the Cypris stage with the rudiment of a disc on the second joint by which the larvae eventually become attached.
By the free Cypris stage, into which the larva next passes, a very complete metamorphosis has been effected. The median and paired eyes are present as before, but the dorsal shield has become a bivalve shell, the two valves of which are united along their dorsal, anterior, and posterior margins. The two valves are further kept in place by an adductor muscle situated close below the mouth. Remains of the lateral horns still persist. The anterior antennae have undergone the metamorphosis already indicated. They are four-jointed, the two basal joints being long, and the second provided with a suctorial disc, in the centre of which is the opening of the duct of the so-called antennary or cement gland, which is a granular mass lying on the ventral side of the anterior region of the body. The gland arises (Willemoes Suhm) during the Nauplius stage in the large upper lip. The two distal joints of the antennae are short, and the last of them is provided with olfactory hairs. The great upper lip and second pair of antennae and mandibles have disappeared, but a small papilla, forming the commencement of the adult mandibles, is perhaps developed in the base of the Nauplius mandibles. The first pair of maxillae have become small papillae and the second pair probably remain. The six posterior pairs of appendages have grown out as functional biramous swimming feet, which can project beyond the shell and are used in the locomotion of the larva. They are composed of two basal joints, and two rami with swimming hairs, each two-jointed. These feet resemble Copepod feet, and form the main ground for the views of Claus and others that the Copepoda and Cirripedia are closely related. They are regarded by Claus as representing the five pairs of natatory feet of Copepoda, and the generative appendages of the segment behind these. Between
the natatory feet are delicate chitinous lamellae, in the spaces between which the cirriform feet of the adult become developed. The ventral spinous process of the Nauplius stage is much reduced, though usually three-jointed. It becomes completely aborted after the larva is fixed.
In addition to the antennary gland there is present, near the dorsal side of the body above the natatory feet, a peculiar paired glandular mass, the origin of which has not been clearly made out, but which is perhaps equivalent to the entomostracan shell gland. It probably supplies the material for the shell in succeeding stages 1 .
The free Cypris stage is not of long duration ; and during it the larva does not take food. It is succeeded by a stage known as the pupa stage (fig. 232 B), in which the larva becomes fixed, while underneath the larval skin the adult structures are developed. This stage fully deserves its name, since it is a quiescent stage during which no nutriment is taken. The attachment takes place by the sucker of the antennae, and the cement gland (/) supplies the cementing material for effecting it. A retrogressive metamorphosis of a large number of the organs sets in, while at the same time the formation of new adult structures is proceeded with. The eyes become gradually lost, but the Nauplius eye is retained,though in a rudimentary state, and the terminal joints of the antennae with their olfactory hairs are thrown off. The bivalve shell is moulted about the same time as the eyes, the skin below it remaining as the mantle. The caudal process becomes aborted. Underneath the natatory
FIG. 232. LARVAL FORMS OF THE THORACICA. (From Huxley.)
A. Nauplius of Balanus balanoides. (After Sp. Bate.) B. Pupa stage of Lepas australis. (After Darwin.)
n. antennary apodemes ; /. cement gland with duct to antenna.
1 There is considerable confusion about the shell gland and antennary gland. In my account Willemoes Suhm has been followed. Claus however regards what I have called the antennary gland as the shell gland, and states that it does not open into the antennae till a later period. He does not clearly describe its opening, nor the organ which I have called the shell gland.
B. II. 32
feet, and between the above-mentioned chitinous lamellae, the cirriform feet are formed ; and on their completion the natatory feet become thrown off and replaced by the permanent feet. In the Lepadidae, in which the metamorphosis of the pupa stages has been most fully studied, the anterior part of the body with the antennae gradually grows out into an elongated stalk, into which pass the ovaries, which are formed during the Cypris stage. At the base of the stalk is the protuberant mouth, the appendages of which soon attain a higher development than in the Cypris stage. At the front part of it a large upper lip becomes formed. Above the mantle and between it and the shell there are formed in the Lepadidae the provisional valves of the shell. These valves are chitinous, and have a fenestrated structure, owing to the chitin being deposited round the margin of the separate epidermis (hypodermis) cells. These valves in the Lepadidae " prefigure in shape, size, and direction of growth, the shelly valves to be formed under and around them" (Darwin, No. 519, p. 129).
Whatever may be the number of valves in the adult the provisional valves never exceed five, viz. the two scuta, the two terga and the carina. They are relatively far smaller than the permanent valves and are therefore separated by considerable membranous intervals. They are often preserved for a long time on the permanent calcareous valves. In the Balanidce the embryonic valves are membranous and do not overlap, but do not present the peculiar fenestrated structure of the primordial valves of the Lepadidae.
In connection with the moult of the pupa skin, and the conversion of the pupa into the adult form, a remarkable change in the position takes place. The pupa lies with the ventral side parallel to and adjoining the surface of attachment, while the long axis of the body of the young Cirriped is placed nearly at right angles to the surface of attachment. This change is connected with the ecdyses of the antennary apodemes (), which leave a deep bay on the ventral surface behind the peduncle. The chitinous skin of the Cirriped passes round the head of this bay, but on the moult of the pupa skin taking place becomes stretched out, owing to the posterior part of the larva bending dorsalwards. It is this flexure which causes the change in the position of the larva.
In addition to the remarkable external metamorphosis undergone during the pupa stage, a series of hardly less considerable internal changes take place, such as the atrophy of the muscles of the antennae, a change in the position of the stomach, etc.
Abdominalia. In the Alcippidae the larva leaves the egg as a Nauplius, and this stage is eventually followed by a pupa stage closely resembling that of the Thoracica. There are six pairs of thoracic natatory legs (Darwin, No. 519). Of these only the first and the last three are preserved in the adult, the first being bent forward in connection with the mouth. The body moreover partially preserves its segmentation, and the mantle does not secrete calcareous valves.
The very remarkable genus Cryptophialus, the development of which is described by Darwin (No. 519) in his classical memoir, is without a free Nauplius stage. The embryo is at first oval but soon acquires two anterior processes, apparently the first pair of antennae, and a posterior prominence, the abdomen. In a later stage the abdominal prominence disappears, and the antennary processes, within which the true antennas are now visible, are carried more towards the ventral surface. The larva next passes into the free Cypris stage, during which it creeps about the mantle cavity of its parent. It is enveloped in a bivalve shell, and the antennae have the normal cirriped structure. There are no other true appendages, but posteriorly three pairs of bristles are attached to a rudimentary abdomen. Paired compound eyes are present. During the succeeding pupa stage the metamorphosis into the adult form takes place, but this has not been followed out in detail.
In Kochlorine, a form discovered by Noll (No. 526) and closely related to Cryptophialus, the larvae found within the mantle represent apparently two larval stages, similar to two of the larval stages described by Darwin.
Rhizocephala. The Rhizocephala, as might have been antici
FIG. 233. STAGES IN THE DEVELOPMENT OF THE RHIZOCEPHALA. (From Huxley, after Fritz Miiller.)
A. Nauplius of Sacculina purpurea. B. Cypris stage of Lernseodiscus porcellanae. C. Adult of Peltogaster paguri.
II, III. IV. Two pairs of antennae and mandibles; cp. carapace; a. anterior end of body; b. generative aperture; c. root-like processes.
pated from their close relationship to Anelasma squalicola amongst the Thoracica, undergo a development differing much less from the type of the Thoracica than that of Cryptophialus and Kochlorine.
Sacculina leaves the egg as a Nauplius (fig. 233 A), which differs from the ordinary type mainly (i) in the large development of an oval dorsal shield (eft] which projects far beyond the edge of the body, but is provided with the typical sternal horns, etc. ; and (2) in the absence of a mouth. The Cypris and pupa stages of Sacculina and other Rhizocephala (fig. 233 B) are closely similar to those of the Thoracica, but the paired eye is absent. The attachment takes place in the usual way, but the subsequent metamorphosis leads to the loss of the thoracic feet and generally to retrogressive changes.
Our knowledge of the development of this remarkable group is entirely due to the investigations of Claus.
Some forms of Cythere are viviparous, and in the marine form Cypridina the embryo develops within the valves of the shell. Cypris attaches its eggs to water plants. The larvae of Cypris are free, and their development is somewhat complicated. The whole development is completed in nine ecdyses, each of them accompanied by more or less important changes in the constitution of the larva.
In the earliest free stage the larva has the characters of a true Nauplius with three pairs of appendages (fig. 234 A). The Nauplius presents howB A
FlG. 234. TWO STAGES IN THE DEVELOPMENT OF CYPRIS. (From ChlUS.)
A. Earliest (Nauplius) stage. B. Second stage.
A'. A". First and second pairs of antennae ; Md. mandibles ; OL. labrum ; MX,', first pair of maxilla; /". first pair of feet.
ever one or two very marked secondary characters. In the first place it is completely enveloped in a fully formed bivalve shell, differing in unessential points from the shell of the adult. An adductor muscle (SM] for the shell is present. Again the second and third appendages, though locomotive in function are neither of them biramous, and the third one already contains a rudiment of the future mandibular blade, and terminates in an anteriorly directed hook-like bristle. The first pair of antenna? is moreover very similar to the second and is used in progression. Neither of the pairs of
antennae become much modified in the subsequent metamorphosis. The Nauplius has a single median eye, as in the adult Cypris, and a fully developed alimentary tract.
The second stage (fig. 234 B), inaugurated by the first moult, is mainly characterized by the appearance of two fresh pairs of appendages, viz. the first pair of maxillae and the first pair of feet ; the second pair of maxillae not being developed till later. The first pair appear as leaf-like curved
FIG. 235. STAGES IN THE DEVELOPMENT OF CYPRIS. (From Claus.)
A. Fourth stage. B. Fifth stage.
MX', first maxilla ; MX", and/', second maxilla ; /". first pair of feet ; L. liver.
plates (Mx'} more or less like Phyllopod appendages (Claus) though at this stage without an exopodite. The first pair of feet (/"} terminates in a curved claw and is used for adhering. The mandibles have by this stage fully developed blades, and have practically attained their adult form, consisting of a powerful toothed blade and a four-jointed palp.
During the third and fourth stages the first pair of maxillae acquire their pectinated gill plate (epipodite) and four blades ; and in the fourth stage (fig. 235 A) the second pair of maxillae (Mx"} arises, as a pair of curved plates, similar to the first pair of maxillae at their first appearance. The forked tail is indicated during the fourth stage by two bristles. During the fifth stage (fig. 235 B) the number of joints of the first pair of antennae becomes increased, and the posterior maxillae develop a blade and become
PHYLOGENY OF THE CRUSTACEA.
four-jointed ambulatory appendages terminating in a hook. The caudal fork becomes more distinct.
In the sixth stage (fig. 236) the second and hindermost pair of feet becomes formed (/"') and the maxillae of the second pair lose their ambulatory function, and begin to be converted into definite masticatory appendages by the reduced jointing of their palp, and the increase of their cutting blades. By the seventh stage all the appendages have practically attained their
FIG. 236. SIXTH STAGE IN THE DEVELOPMENT OF CYPRIS. (From Claus.) MX!, first maxilla ; Mx".f. second maxilla; /'. and/"', first and second pair oi feet ; Fu. caudal fork ; L. liver ; S.D. shell gland.
permanent form ; the second pair of maxillae has acquired small branchial plates, and the two following feet have become jointed. In the eighth and ninth stages the generative organs attain their mature form.
The larva of Cythere at the time of birth has rudiments of all the limbs, but the mandibular palp still functions as a limb, and the three feet (2nd pair of maxillae and two following appendages) are very rudimentary.
The larvae of Cypridina are hatched in a condition which to all intents and purposes resembles the adult.
Phylogeny of the Crustacea.
The classical work of Fritz Miiller (No. 452) on the phylogeny of the Crustacea has given a great impetus to the study of their larval forms, and the interpretations of these forms which he has offered have been the subject of a very large amount of criticism and discussion. A great step forward in this discussion has been recently made by Claus in his memoir (No. 448).
The most fundamental question concerns the meaning of the Nauplius. Is the Nauplius the ancestral form of the Crustacea, as is believed by Fritz Miiller and Claus, or are its peculiarities and constant occurrence due to some other cause ? The most plausible explanation on the second hypothesis
would seem to be the following. The segments with their appendages of Arthropoda and Annelida are normally formed from before backwards, therefore every member of these two groups with more than three segments must necessarily pass through a stage with only three segments, and the fact that in a particular group this stage is often reached on the larva being hatched is in itself no proof that the ancestor of the group had only three segments with their appendages. This explanation appears to me, so far as it goes, quite valid ; but though it relieves us from the necessity of supposing that the primitive Crustacea had only three pairs of appendages, it does not explain several other peculiarities of the Nauplius 1 . The more important of these are the following.
1. That the mandibles have the form of biramous swimming feet and are not provided with a cutting blade.
2. That the second pair of antennae are biramous swimming feet with a hook used in mastication, and are innervated (?) from the subcesophageal ganglion.
3. The absence of segmentation in the Nauplius body. An absence which is the more striking in that before the Nauplius stage is fully reached the body of the embryo is frequently divided into three segments, e.g. Copepoda and Cirripedia
4. The absence of a heart.
5. The presence of a median single eye as the sole organ of vision.
Of these points the first, second, and fifth appear only to be capable of being explained phylogenetically, while with reference to the absence of a heart it appears very improbable that the ancestral Crustacea were without a central organ of circulation. If the above positions are accepted the conclusion would seem to follow that in a certain sense the Nauplius is an ancestral form but that, while it no doubt had its three anterior pairs of appendages similar to those of existing Nauplii, it may perhaps have been provided with a segmented body behind provided with simple biramous appendages. A heart and cephalo-thoracic shield may also have been present, though the existence of the latter is perhaps doubtful. There was no doubt a median single eye, but it is difficult to decide whether or no paired compound eyes were also present. The tail ended in a fork between the prongs of which the anus opened ; and the mouth was protected by a large upper lip. In fact, it may very probably turn out that the most primitive Crustacea more resembled an Apus larva at the moult immediately before the appendages lose their Nauplius characters (fig. 208 B), or a Cyclops larva just before the Cyclops stage (fig. 229), than the earliest Nauplius of either of these forms.
If the Nauplius ancestor thus reconstructed is admitted to have existed, the next question in the phylogeny of the Crustacea concerns the relations of the various phyla to the Nauplius. Are the different phyla descended from the Nauplius direct, or have they branched at a later period from
1 For the characters of Nauplius vide p. 460.
504 PHYLOGENY OF THE CRUSTACEA.
some central stem? It is perhaps hardly possible as yet to give a full and satisfactory answer to this question, which requires to be dealt with for each separate phylum ; but it may probably be safely maintained that the existing Phyllopods are members of a group which was previously much larger, and the most central of all the Crustacean groups; and which more nearly retains in the characters of the second pair of antennae etc. the Nauplius peculiarities. This view is shared both by Claus and Dohrn, and appears to be in accordance with all the evidence we have both palaeontological and morphological. Claus indeed carries this view still further, and believes that the later Nauplius stages of the different Entomostracan groups and the Malacostraca (Penaeus larva) exhibit undoubted Phyllopod affinities. He therefore postulates the earlier existence of a Protophyllopod form, which would correspond very closely with the Nauplius as reconstructed above, from which he believes all the Crustacean groups to have diverged.
It is beyond the scope of this work to attempt to grapple with all the difficulties which arise in connection with the origin and relationships of the various phyla, but I confine myself to a few suggestions arising out of the developmental histories recorded above.
Malacostraca. In attempting to reconstitute from the evidence in our possession the ancestral history of the Malacostraca we may omit from consideration the larval history of all those types which leave the egg in nearly the adult form, and confine our attention to those types in which the larval history is most completely preserved.
There are three forms which are of special value in this respect, viz. Euphausia, Penaeus and Squilla. From the history of these which has already been given it appears that in the case of the Decapoda four stages (Claus) may be traced in the best preserved larval histories.
1. A Nauplius stage with the usual Nauplius characters.
2. A Protozoaea stage in which the maxillae and first pair of maxillipeds are formed behind the Nauplius appendages ; but in which the tail is still unsegmented. This stage is comparatively rarely preserved and usually not very well marked.
3. A Zoaea stage the chief features of which have already been fully characterised (vide p. 465). Three more or less distinct types of Zosea are distinguished by Claus. (a) That of Penaeus, in which the appendages up to the third pair of maxillipeds are formed, and the thorax and abdomen are segmented, the former being however very short. The heart is oval, with one pair of ostia. From this type the Zoaea forms of the other Decapoda are believed by Claus to be derived, (b} That of Euphausia, with but one pair of maxillipeds and those short and Phyllopod-like. The heart oval with one pair of ostia. (c) That of Squilla, with an elongated manychambered heart, two pairs of maxillipeds and the abdominal appendages in full activity.
4. A Mysis stage, which is only found in the macrurous Decapod larvie.
The embryological questions requiring to be settled concern the value
of the above stages. Do they represent stages in the actual evolution of the present types, or have their characters been secondarily acquired in larval life ?
With reference to the first stage this question has already been discussed, and the conclusion arrived at, that the Nauplius does in a much modified form represent an ancestral type. As to the fourth stage there can be no doubt that it is also ancestral, considering that it is almost the repetition of an actually existing form.
The second stage can clearly only be regarded as an embryonic preparation for the third ; and the great difficulty concerns the third stage.
The natural view is that this stage like the others has an ancestral value, and this view was originally put forward by Fritz Miiller and has been argued for also by Dohrn. On the other hand the opposite side has been taken by Claus, who has dealt with the question very ably and at great length, and has clearly shewn that some of Fritz Miiller's positions are untenable. Though Claus' opinion is entitled to very great weight, an answer can perhaps be given to some of his objections. The view adopted in this section can best be explained by setting forth the chief points which Claus urges against Fritz Miiller's view.
The primary question which needs to be settled is whether the Malacostraca have diverged very early from the Nauplius root, or later in the history of the Crustacea from the Phyllopod stem. On this question Claus 1 brings arguments, which appear to me very conclusive, to shew that the Malacostraca are derived from a late Protophyllopod type, and Claus' view on this point is shared also by Dohrn. The Phyllopoda present so many characters (not possessed by the Nauplius) in common with the Malacostraca or their larval forms, that it is incredible that the whole of these should have originated independently in the two groups. The more important of these characters are the following.
1. The compound eyes, so often stalked in both groups.
2. The absence of a palp on the mandible, a very marked character of the Zoasa as well as of the Phyllopoda.
3. The presence of a pair of frontal sense knobs.
4. The Phyllopod character of many of the appendages. Cf. first pair of maxillipeds of the Euphausia Zosea.
1 Claus speaks of the various Crustacean phyla as having sprung from a Protophyllopod form, and it might be supposed that he considered that they all diverged from the same form. It is clear however from the context that he regards the Protophyllopod type from which the Malacostraca originated as far more like existing Phyllopods than that from which the Entomostracan groups have sprung. It is not quite easy to get a consistent view of his position on the question, since he states (p. 77) that the Malacostraca and the Copepods diverged from a similar form, which is represented in their respective developments by the Protozosea and earliest Cyclops stage. Yet if I understand him rightly, he does not consider the Protozosea stage to be the Protophyllopod stage from which the Malacostraca have diverged, but states on p. 71 that it was not an ancestral form at all.
506 PHYLOGENY OF THE CRUSTACEA.
5. The presence of gill pouches (epipodites) on many of the appendages 1 .
In addition to these points, to which others might be added, Claus attempts to shew that Nebalia must be regarded as a type intermediate between the Phyllopods and Malacostraca. This view seems fairly established, and if true is conclusive in favour of the Phyllopod origin of the Malacostraca. If the Protophyllopod origin of the Malacostraca is admitted, it seems clear that the ancestral forms of the Malacostraca must have developed their segments regularly from before backwards, and been provided with nearly similar appendages on all the segments. This however is far from the case in existing Malacostraca, and Fritz Miiller commences his summary of the characters of the Zoaea in the following words 2 . "The middle body with its appendages, those five pairs of feet to which these animals owe their name, is either entirely wanting or scarcely indicated." This he regards as an ancestral character of the Malacostraca, and is of opinion that their thorax is to be regarded as a later acquirement than the head or abdomen. Claus' answer on this point is that in the most primitive Zoasas, viz. those already spoken of as types, the thoracic and abdominal segments actually develop, in regular succession from before backwards, and he therefore concludes that the late development of the thorax in the majority of Zoaea forms is secondary and not an ancestral Phyllopod peculiarity.
This is the main argument used by Claus against the Zosea having any ancestral meaning. His view as to the meaning of the Zoaea may be gathered from the following passage. After assuming that none of the existing Zoaea types could have been adult animals, he says" Much more "probably the process of alteration of the metamorphosis, which the Mala" costracan phylum underwent in the course of time and in conjunction " with the divergence of the later Malacostracan groups, led secondarily " to the three different Zoaea configurations to which probably later modifica" tions were added, as for instance in the young form of the Cumaceae. We "might with the same justice conclude that adult Insects existed as cater" pillars or pupae as that the primitive form of the Malacostraca was a " Protozoaea or Zoaea."
Granting Claus' two main positions, viz. that the Malacostraca are derived from Protophyllopods, and that the segments were in the primary ancestral forms developed from before backwards, it does not appear impossible that a secondary and later ancestral form may have existed with a reduced thorax. This reduction may only have been partial, so that the Zoaea ancestor would have had the following form. A large cephalo-thorax and well-developed tail (?) with swimming appendages. The appendages up to the second pair of maxillipeds fully developed, but the thorax very
1 Claus appears to consider it doubtful whether the Malacostracan gills can be compared with the Phyllopod gill-pouches. 3 Facts for Darwin, p. 49.
imperfect and provided only with delicate foliaceous appendages not projecting beyond the edge of the cephalo-thoracic shield.
Another hypothesis for which there is perhaps still more to be said is that there was a true ancestral Zoaea stage in which the thoracic appendages were completely aborted. Claus maintains that the Zoaea form with aborted thorax is only a larval form ; but he would probably admit that its larval characters were acquired to enable the larva to swim better. If this much be admitted it is not easy to see why an actual member of the ancestral series of Crustacea should not have developed the Zoaea peculiarities when the mud-dwelling habits of the Phyllopod ancestors were abandoned, and a swimming mode of life adopted. This view, which involves the supposition that the five (or six including the third maxillipeds) thoracic appendages were lost in the adult (for they may be supposed to have been retained in the larva) for a series of generations, and reappeared again in the adult condition, at a later period, may at first sight appear very improbable, but there are, especially in the larval history of the Stomatopoda, some actual facts which receive their most plausible explanation on this hypothesis.
These facts consist in cases of the actual loss of appendages during development, and their subsequent reappearance. The two most striking cases are the following.
1. In the Erichthus form of the Squilla larva the appendages corresponding to the third pair of maxillipeds and first two pairs of ambulatory appendages of the Decapoda are developed in the Protozosea stage, but completely aborted in the Zoasa stage, and subsequently redeveloped.
2. In the case of the larva of Sergestes in the passage from the Acanthosoma (Mysis) stage to the Mastigopus stage the two hindermost thoracic appendages become atrophied and redevelop again later.
Both of these cases clearly fit in very well with the view that there was an actual period in the history of the Malacostraca in which the ancestors of the present forms were without the appendages which are aborted and redeveloped again in these larval forms. Claus' hypothesis affords no explanation of these remarkable cases.
It is however always possible to maintain that the loss and reappearance of the appendages in these cases may have no ancestral meaning ; and the abortion of the first pair of maxillipeds and reduction of some of the other appendages in the case of the Loricata is in favour of this explanation. Similar examples of the abortion and reappearance of appendages, which cannot be explained in the way attempted above, are afforded by the Mites and also by the Insects, e.g. Bees.
On the other hand there is almost a conclusive indication that the loss of the appendages in Sergestes has really the meaning assigned to it, in that in the allied genius Leucifer the two appendages in question are actually absent in the adult, so that the stage with these appendages absent is permanently retained in an adult form. In the absence of the mandibular palp in all the Zoaea forms, its actual atrophy in the Penaeus Zoasa, and its
508 PHYLOGENY OF THE CRUSTACEA.
universal reappearance in adult Malacostraca, are cases which tell in favour of the above explanation. The mandibular palp is permanently absent in Phyllopods, which clearly shews that its absence in the Zoaea stage is due to the retention of an ancestral peculiarity, and that its reappearance in the adult forms was a late occurrence in the Malacostracan history.
The chief obvious difficulty of this view is the redevelopment of the thoracic feet after their disappearance for a certain number of generations. The possibility of such an occurrence appears to me however clearly demonstrated by the case of the mandibular palp, which has undoubtedly been reacquired by the Malacostraca, and by the case of the two last thoracic appendages of Sergestes just mentioned. The above difficulty may be diminished if we suppose that the larvae of the Zoaea ancestors always developed the appendages in question. Such appendages might first only partially atrophy in a particular Zoaea form and then gradually come to be functional again ; so that, as a form with functional thoracic limbs came to be developed out of the Zoaea, we should find in the larval history of this form that the limbs were developed in the pre-zoaeal larval stages, partially atrophied in the Zoaea stage, and redeveloped in the adult. From this condition it would not be difficult to pass to a further one in which the development of the thoracic limbs became deferred till after the Zoaea stage.
The general arguments in favour of a Zoaea ancestor with partially or completely aborted thoracic appendages having actually existed in the past appear to me very powerful. In all the Malacostracan groups in which the larva leaves the egg in an imperfect form a true Zoaea stage is found. That the forms of these Zoaeas should differ considerably is only what might be expected, considering that they lead a free existence and are liable to be acted upon by natural selection, and it is probable that none of those at present existing closely resemble the ancestral form. The spines from their carapace, which vary so much, were probably originally developed, as suggested by Fritz Miiller, as a means of defence. The simplicity of the heart so different from that of Phyllopods in most forms of Zoaea is a difficulty, but the reduction in the length of the heart may very probably be a secondary modification ; the primitive condition being retained in the Squilla Zoaea. In any case this difficulty is not greater on the hypothesis of the Zoaea being an ancestral form, than on that of its being a purely larval one.
The points of agreement in the number and character of the appendages, form of the abdomen, etc. between the various types of Zoaea appear to me too striking to be explained in the manner attempted by Claus. It seems improbable that a peculiarity of form acquired by the larva of some ancestral Malacostracan should have been retained so permanently in so many groups l
1 A secondary larval form is less likely to be repeated in development than an ancestral adult stage, because there is always a strong tendency for the former, which is a secondarily intercalated link in the chain, to drop out by the occurrence of a reversion to the original type of development.
more permanently indeed than undoubtedly ancestral forms like that of Mysis and it would be still more remarkable that a Zoaea form should have been two or more times independently developed.
There are perhaps not sufficient materials to reconstruct the characters of the Zoaea ancestor, but it probably was provided with the anterior appendages up to the second pair of maxillipeds, and (?) with abdominal swimming feet. The heart may very likely have been many-chambered. Whether gill pouches were present on the maxillipeds and abdominal feet does not appear to me capable of being decided. The carapace and general shape were probably the same as in existing Zoaeas. It must be left an open question whether the six hindermost thoracic appendages were absent or only very much reduced in size.
On the whole then it may be regarded as probable that the Malacostraca are descended from Protophyllopod forms, in which, on the adoption of swimming habits, six appendages of the middle region of the body were reduced or aborted, and a Zoaea form acquired, and that subsequently the lost appendages were redeveloped in the descendants of these forms, and have finally become the most typical appendages of the group.
The relationship of the various Malacostracan groups is too difficult a subject to be discussed here, but it seems to me most likely that in addition to the groups with a Zoaea stage the Edriophthalmata and Cumaceae are also post-zoaeal forms which have lost the Zoasa stage. Nebalia is however very probably to be regarded as a prae-zoaeal form which has survived to the present day ; and one might easily fancy that its eight thin thoracic segments with their small Phyllopod-like feet might become nearly aborted.
Copepoda. The Copepoda certainly appear to have diverged very early from the main stem, as is shewn by their simple biramous feet and the retention of the median eye as the sole organ of vision. It may be argued that they have lost the eye by retrogressive changes, and in favour of this view cases of the Pontellidae and of Argulus may be cited. It is however more than doubtful whether the lateral eyes of the Pontellidae are related to the compound Phyllopod eye, and the affinities of Argulus are still uncertain. It would moreover be a great paradox if in a large group of Crustacea the lateral eyes had been retained in a parasitic form only (Argulus), but lost in all the free forms.
Cirripedia. The Cirripedia are believed by Claus to belong to the same phylum as the Copepoda. This view does not appear to be completely borne out by their larval history. The Nauplius differs very markedly from that of the Copepoda, and this is still more true of the Cypris stage. The Copepod-like appendages of this stage are chiefly relied upon to support the above view, but this form of appendages was probably very primitive and general, and the number (without taking into consideration the doubtful case of Cryptophialus) does not correspond to that in Copepoda. On the other hand the paired eyes and the bivalve shell form great difficulties in the way of Claus' view. It is clear that the Cypris stage represents more or less
PHYLOGENY OF THE CRUSTACEA.
closely an ancestral form of the Cirripedia, and that both the large bivalve shell and the compound eyes were ancestral characters. These characters would seem incompatible with Copepod affinities, but point to the independent derivation of the Cirripedia from some early bivalve Phyllopod form.
Ostracoda. The independent origin of the Ostracoda from the main Crustacean stem seems probable. Claus points out that the Ostracoda present by no means a simple organisation, and concludes that they were not descended from a form with a more complex organisation and a larger number of appendages. Some simplifications have however undoubtedly taken place, as the loss of the heart, and of the compound eyes in many forms. These simplifications are probably to be explained (as is done by Claus) as adaptations due to the small size of body and its enclosure in a thick bivalve shell. Although Claus is strongly opposed to the view that
FIG. 737. FIGURES ILLUSTRATING THE DEVELOPMENT OF ASTACUS. (From Parker ; after Reichenbach.)
A. Section through part of the ovum during segmentation, n. nuclei ; w.y. white yolk ; y.p. yolk pyramids ; c. central yolk mass.
B and C. Longitudinal sections during the gastrula stage, a. archenteron ; b. blastopore ; ms. mesoblast ; ec. epiblast ; en. hypoblast distinguished from epiblast by shading.
I '. Highly magnified view of the anterior lip of blastopore to shew the origin of the primary mesoblast from the wall of the archenteron. p.ms. primary mesoblast ; ec. epiblast ; en. hypoblast.
I Two hypoblast cells to shew the amoeba-like absorption of yolk spheres. y. yolk ; . nucleus ; /. pseudopodial process.
F. Hypoblast cells giving rise endogenously to the secondary mesoblast (s.nts.). tt. nuclei.
CRUSTACEA. 5 1
the number of the appendages has been reduced, yet the very fact of the (in some respects) complex organisation of this group might seem to indicate that it cannot have diverged from the Phyllopod stem at so early a stage as (on Claus' view of the Nauplius) would seem to be implied by the very small number of appendages which is characteristic of it, and it therefore appears most probable that the present number may be smaller than that of the ancestral forms.
The formation of the germinal layers.
The formation of the germinal layers has been more fully studied in various Malacostraca, more especially in the Decapoda, than in other groups.
Decapoda. To Bobretzky (No. 472) is due the credit of having been the pioneer in this line of investigation ; and his researches have been followed up and enlarged by Haeckel, Reichenbach (No. 488), and Mayer (No. 482). The segmentation is centrolecithal and regular (fig. 237 A). At its close the blastoderm is formed of a single uniform layer of lens-shaped cells enclosing a central sphere of yolk, in which as a rule all trace of the division into columns, present during the earlier stages of segmentation, has disappeared ; though in Palaemon the columns remain for a long period distinct. The cells of the blastoderm are at first uniform, but in Astacus, Eupagurus, and most Decapoda, soon become more columnar for a small area, and form a circular patch. The whole patch either becomes at once invaginated (Eupagurus, Palaemon, fig. 239 A) or else the edge of it is invaginated as a roughly speaking circular groove deeper anteriorly than posteriorly, within which the remainder of the patch forms a kind of central plug, which does not become invaginated till a somewhat later period (Astacus, fig. 237 B and C). After the invagination of the above patch the remainder of the blastoderm cells form the epiblast.
The invaginated sack appears to be the archenteron and its mouth the blastopore. The mouth finally becomes closed 1 , and the sack itself then forms the mesenteron.
In Astacus the archenteron gradually grows forwards, its opening is at first wide, but becomes continuously narrowed
1 Bobretzky first stated that the invagination remained open, but subsequently corrected himself. Zeit. /. Wiss. Zool., Bd. xxiv. p. 186.
FORMATION OF THE LAYERS.
and is finally obliterated. Very shortly after this occurrence there is formed, slightly in front of the point where the last trace of the blastopore was observable, a fresh epiblastic invagination, which gives rise to the proctodaeum, and the opening of which remains as the definite anus. The proctodaeum (fig. 238 A, kg) is very soon placed in communication with the mesenteron (mg). The stomodaeum (fg) is formed during the same stage as the proctodaeum. It gives rise to the oesophagus and stomach. The hypoblast cells which form the wall of the archenteron grow with remarkable rapidity at the expense of the yolk ; the spherules of which they absorb and digest in an amceba-like fashion by means of their pseudopodia. They become longer and longer, and finally, after absorbing the whole yolk, acquire a form almost exactly similar to that of the yolk pyramids during segmentation (fig. 238 B). They enclose the cavity of the mesenteron, and their nuclei and protoplasm are situated externally. The cells of the mesenteron close to its junction with the proctodaeum differ from those elsewhere in being nearly flat.
In Palaemon (Bobretzky) the primitive invagination (fig. 239 A) has far smaller dimensions than in Astacus, and appears before the blastoderm cells have separated from the yolk pyramids. The cells which are situated at the bottom of it pass into the yolk, increase in number, and absorb the whole yolk, forming a solid mass of hypoblast in which the outlines of the individual cells would seem at first not to be distinct.
FlG. 238. TWO LONGITUDINAL SECTIONS OF THE EMBRYO OF ASTACUS.
(From Parker ; after Bobretzky.)
A. Nauplius stage. B. Stage after the hypoblast cells have absorbed the food yolk. The ventral surface is turned upwards, fg. stomodseum ; hg. proctodccum ; an. anus ; m. mouth ; mg. mesenteron ; abd. abdomen ; h. heart.
The blastopore in the mean
time becomes closed. Some of the nuclei now pass to the periphery of the yolk mass ; the cells appertaining to them gradually become distinct and assume a pyramidal form (fig. 239 B, hy\ the inner ends of the cells losing themselves in a central mass of yolk, in the interior of which nuclei are at first present but soon disappear. The mesenteron thus becomes constituted of a layer of pyramidal cells which merge into a central mass of yolk. Some of the hypoblast cells adjoining the junction of the proctodaeum and mesenteron become flattened, and in the neighbourhood of these cells a lumen
FlG. 239. TWO STAGES IN THE DEVELOPMENT OF PAL^MON SEEN IN SECTION.
A. Gastrula stage.
B. Longitudinal section through a late stage, hy. hypoblast ; sg. supra-resophageal ganglion ; vg. ventral nerve cord ; hd. proctodseum ; st. stomodseum.
first appears. The stomodaeum and proctodaeum are formed as in Astacus. Fig. 239 B shews the relative positions of the proctodaeum, stomodaeum, and mesenteron. Although the process of formation of the hypoblast and mesenteron is essentially the same in Astacus and Palaemon, yet the differences between these two forms are very interesting, in that the yolk is external to the mesenteron in Astacus, but enclosed within it in Palaemon. This difference in the position of the yolk is rendered possible by the fact that the invaginated hypoblast cells in Palaemon do not, at first, form a continuous layer enclosing a central cavity, while they do so in Astacus.
The mesoblast appears to be formed of cells budded off from the anterior wall of the archenteron (Astacus, fig. 237 D), B. II. 33
514 FORMATION OF THE LAYERS.
or from its lateral walls generally (Palaemon). They make their first appearance soon after the imagination of the hypoblast has commenced. The mesoblast cells are at first spherical, and gradually spread, especially in an anterior direction, from their point of origin.
According to Reichenbach there are formed in Astacus at the Nauplius stage a number of peculiar cells which he speaks of as * secondary mesoblast cells.' His account is not very clear or satisfactory, but it appears that they originate (fig. 237 F) in the hypoblast cells by a kind of endogenous growth, and though they have at first certain peculiar characters they soon become indistinguishable from the remaining mesoblast cells.
Towards the end of the Nauplius period the secondary mesoblast cells aggregate themselves into a rod close to the epiblast in the median ventral line, and even bifurcate round the mouth and extend forwards to the extremity of the procephalic lobes. This rod of cells very soon vanishes, and the secondary mesoblast cells become indistinguishable from the primary. Reichenbach believes, on not very clear evidence, that these cells have to do with the formation of the blood.
General form of the body. The ventral thickening of epitlast or ventral plate, continuous with the invaginated patch already mentioned, forms the first indication of the embryo. It is at first oval, but soon becomes elongated and extended anteriorly into two lateral lobes the procephalic lobes. Its bilateral symmetry is further indicated by a median longitudinal furrow. The posterior end of the ventral plate next becomes raised into a distinct lobe the abdomen which in Astacus at first lies in front of the still open blastopore. This lobe rapidly grows in size, and at its extremity is placed the narrow anal opening. It soon forms a well-marked abdomen bent forwards over the region in front (figs. 239 B, and 240 A and B). Its early development as a distinct outgrowth causes it to be without yolk ; and so to contrast very forcibly with the anterior thoracic and cephalic regions of the body. In most cases this process corresponds to the future abdomen, but in some cases (Loricata) it appears to include part of the thorax. Before it has reached a considerable development, three pairs of appendages spring from the region of the head, viz. two pairs of antennae and the mandibles, and inaugurate a so-called Nauplius stage (fig. 240 A). These three appendages are formed nearly simultaneously, but the hindermost appears to become visible slightly before the two others
(Bobretzky). The mouth lies slightly behind the anterior pair of antennae, but distinctly in front of the posterior pair. The other appendages, the number of which at the time of hatching varies greatly in the different Decapods (vide section on larval development), sprout in succession from before backwards (fig. 240 B). The food yolk in the head and thoracic region gradually becomes reduced in quantity with the growth of the embryo, and by the time of hatching the disparity in size between the thorax and abdomen has ceased to exist.
Isopoda. The early embryonic phases of the Isopoda have been studied by means of sections by Bobretzky (No. 498) and Bullar (No. 499) and have been found to present considerable
FlG. 240. TWO STAGES IN THE DEVELOPMENT OF
A. Nauplius stage.
B. Stage with eight pairs of appendages, op. eyes ; at 1 , and at*, first and second antennae; md. mandibles; mx l , mx 2 . first and second maxillae; mxp*. third maxillipeds ; Ib. upper lip.
variations. When laid the egg is enclosed in a chorion, but shortly after the commencement of segmentation (Ed. van Beneden and Bullar) a second membrane appears, which is probably of the nature of a larval membrane.
In all the forms the segmentation is followed by the formation of a blastoderm, completely enclosing the yolk, and thickened along an area which will become the ventral surface of the embryo. In this area the blastoderm is formed of at least two layers of cells an external columnar epiblast, and an internal layer of scattered cells which form the mesoblast and probably in part also the hypoblast (Oniscus, Bobretzky ; Cymothoa, Bullar).
516 FORMATION OF THE LAYERS.
In Asellus aquaticus there is a centrolecithal segmentation, ending in the formation of a blastoderm, which appears first on the ventral surface and subsequently extends to the dorsal.
In Oniscus murarius, and Cymothoa the segmentation is partial [for its peculiarities and relationship vide p. 120] and a disc, formed of a single layer of cells, appears at a pole of the egg which corresponds to the future ventral surface (Bobretzky). This layer gradually grows round the yolk partly by division of its cells, though a formation of fresh cells from the yolk may also take place. Before it has extended far round the yolk, the central part of it becomes two or more layers deep, and the cells of the deeper layers rapidly increase in number, and are destined to give rise to the mesoblast and probably also to part or the whole of the hypoblast. In Cymothoa this layer does not at first undergo any important change, but in Oniscus it becomes very thick, and its innermost cells (Bobretzky) become imbedded in the yolk, which they rapidly absorb; and increasing in number first of all form a layer in the periphery of the yolk, and finally fill up the whole of the interior of the yolk (fig. 241 A), absorbing it in the process.
It appears possible that these cells do not, as Bobretzky believes, originate from the blastoderm, but from nuclei in the yolk which have escaped his observation. This mode of origin would be similar to that by which yolk cells originate in the eggs of the Insecta, etc. If Bobretzky's account is correct we must look to Palaemon, as he himself suggests, to find an explanation of the passage of the hypoblast cells into the yolk. The thickening of the primitive germinal disc would, according to this view, be equivalent to the invagination of the archenteron in Astacus, Palaemon, etc.
Whatever may be the origin of the cells in the yolk they no doubt correspond to the hypoblast of other types. In Cymothoa nothing similar to them has been met with, but the hypoblast has a somewhat different origin ; being apparently formed from some of the indifferent cells below the epiblast, which collect as a solid mass on the ventral surface, and then divide into two masses which become hollow and give rise to the liver caeca. Their fate, as well as that of the hypoblast in Oniscus, is dealt with in connection with the alimentary tract. The completion of the enclosure of the yolk by the blastoderm takes place on the dorsal surface. In all the Isopods which have been carefully
studied, there appears before any other organ a provisional structure formed from the epiblast and known as the dorsal organ. An account of it is given in connection with the development of the organs. The general external changes undergone by the larva in its development are as follows. The ventral thickened area of the blastoderm (ventral plate) shapes itself and girths nearly the whole circumference of the ovum in Oniscus (fig. 241 A) but is relatively much shorter in Cymothoa. Anteriorly it dilates into the two procephalic lobes. In Cymothoa it next becomes segmented; and the anterior segments are formed nearly simultaneously, and those of the abdomen somewhat later. At the same time a median depres
FlG. 241. TWO LONGITUDINAL SECTIONS THROUGH THE EMBRYO OF ONISCUS
MURARIUS. (After Bobretzky.)
st. stomodaeum ; pr. proctodseum ; hy. hypoblast formed of large nucleated cells imbedded in the yolk ; m. mesoblast ; vg. ventral nerve cord ; sg. supra- oesophageal ganglion ; li. liver ; do. dorsal organ ; zp. rudiment of masticatory apparatus ; ol. upper lip.
sion appears dividing the blastoderm longitudinally into two halves. The appendages are formed later than their segments, and the whole of them are formed nearly simultaneously, with the exception of the last thoracic, which does not appear till comparatively late after the hatching of the embryo. The late development of the seventh thoracic segment and appendage is a feature common to the majority of the Isopoda (Fritz Miiller). In Oniscus the limbs are formed in nearly the same way as in Cymothoa, but in Asellus they do not arise quite simultaneously. First of all, the two antennae and mandibles (the future palp) appear, inaugurating a stage often spoken of as the Nauplius stage, which is supposed to correspond with the free Nauplius
5l8 FORMATION OF THE LAYERS.
stage of Penaeus and Euphausia. At this stage a cuticle is shed (Van Beneden) which remains as an envelope surrounding the larva till the time of hatching. Similar cuticular envelopes are formed in many Isopoda. Subsequently the appendages of the thorax appear, and finally those of the abdomen. Later than the appendages there arise behind the mouth two prominences which resemble appendages, but give rise to a bilobed lower lip (Dohrn).
In Asellus and Oniscus the ventral plate moulds itself to the shape of the egg, and covers the greater part of the dorsal as well as of the ventral side (fig. 241 A). As a result of this the ventral surface of the embryo is throughout convex ; and in Asellus a deep fold appears on the back of the embryo, so that the embryo appears coiled up within the egg with its ventral side outwards and its head and tail in contact. In Oniscus the ventral surface is convex, but the dorsal surface is never bent in as in Asellus. In Cymothoa the egg is very big and the ventral plate does not extend nearly so far round to the dorsal side as in Asellus, in consequence of which the ventral surface is not nearly so convex as in other Isopoda. At the same time the telson is early formed, and is bent forwards so as to lie on the under side of the part of the blastoderm in front. In having this ventral curvature of the telson Cymothoa forms an exception amongst Isopods ; and in this respect is intermediate between the embryos of Asellus and those of the Amphipoda.
Amphipoda. Amongst the Amphipoda the segmentation is usually centrolecithal. In the case of Gammarus locusta (Ed. van Beneden and Bessels, No. 503) it commences with an unequal but total segmentation like that of the Frog (vide p. 97), and the separation of a central yolk mass is a late occurrence ; and it is noticeable that the part of the egg with the small segments eventually becomes the ventral surface. In the fresh-water species of Gammarus (G. pulex and fluviatilis) the segmentation is more like that of Insects ; the blastoderm cells being formed nearly simultaneously over a large part of the surface of the egg.
Both forms of segmentation give rise to a blastoderm covering the whole egg, which soon becomes thickened on the ventral
surface. There is formed, as in the Isopoda, a larval membrane at about the time when the blastoderm is completed. Very soon after this the egg loses its spherical shape, and becomes produced into a pointed extremity the future abdomen which is immediately bent over the ventral surface of the part in front. The ventral curvature of the hinder part of the embryo at so early an age stands in marked contrast to the usual condition of Isopod embryos, and is only approached in this group, so far as is known, in the case of Cymothoa.
At the formation of the first larval membrane the blastoderm cells separate themselves from it, except at one part on the dorsal surface. The patch of cells adherent at this part gives rise to a dorsal organ, comparable with that in Oniscus, connecting the embryo and its first larval skin. A perforation appears in it at a later period.
The segments and limbs of the Amphipoda are all formed before the larva leaves the egg.
Cladocera. The segmentation (Grobben, No. 455) takes place on the normal centrolecithal type, but is somewhat unequal. Before the close of the segmentation there may be seen at the apex of the vegetative pole one cell marked off from the remainder by its granular aspect. It gives rise to the generative organs. One of the cells adjoining it gives rise to the hypoblast, and the other cells which surround it form the commencement of the mesoblast. The remaining cells of the ovum form the epiblast. By a later stage the hypoblast cell is divided into thirty-two cells and the genital cell into four, while the mesoblast forms a circle of twelve cells round the genital mass.
The hypoblast soon becomes involuted ; the blastopore probably closes, and the hypoblast forms a solid cord of cells which eventually becomes the mesenteron. The stomodaeum is said to be formed at the point of closure of the blastopore. The mesoblast passes inwards and forms a mass adjoining the hypoblast, and somewhat later the genital mass also becomes covered by the epiblast. The proctodseum appears to be formed later than the stomodasum.
The embryo as first shewn by Dohrn passes through a Nauplius stage in the brood-pouch, but is hatched, except in the case of the winter eggs of Leptodora, in a form closely resembling the adult.
Copepoda. Amongst the free Copepoda the segmentation and formation of the layers have recently been investigated by Hoek (No. 512). He finds that there is, in both the fresh-water and marine forms studied by him, a centrolecithal segmentation similar to that of Palaemon and Pagurus (vide p. 112), which might from the surface be supposed to be
520 FORMATION OF THE LAYERS.
complete and nearly regular. After the formation of the blastoderm an invagination of some of its cells takes place and is completed in about a quarter of an hour. The opening becomes closed. This invagination is compared by Hoek to the invagination in Astacus, and is believed by him to give rise to the mesenteron. Its point of closing corresponds with the hind end of the embryo. On the ventral surface there appear two transverse furrows dividing the embryo into three segments, and a median longitudinal furrow which does not extend to the front end of the foremost segment. The three pairs of Nauplius appendages and upper lip become subsequently formed as outgrowths from the sides of the ventral blastodermic thickening.
Amongst the parasitic Copepoda there are found two distinct types of segmentation, analogous to those in the Isopoda. In the case of Condracanthus the segmentation is somewhat irregular, but on the type of Eupagurus, etc. (vide p. 112). In the other group (Anchorella, Clavella, Congericola, Caligus, Lerneopoda) the segmentation nearly resembles the ordinary meroblastic type (vide p. 120), and is to be explained in the same manner as in the cases of Oniscus and Cymothoa. The first blastodermic cells sometimes appear in a position corresponding with the head end of the embryo (Anchorella), at other times at the hind end (Clavella), and sometimes in the middle of the ventral surface. The dorsal surface of the yolk is always the latest to be inclosed by the blastoderm cells. A larval cuticle similar to that of the Isopoda is formed at the same time as the blastoderm. At the sides of the ventral thickening of the blastoderm there grow out the Nauplius appendages, of which only the first two appear in Anchorella. In Anchorella and Lerneopoda the embryos are not hatched at the Nauplius stage, but after the Nauplius appendages have been formed a fresh cuticle the Nauplius cuticle is shed, and within it the embryo develops till it reaches the so-called Cyclops stage (vide p. 490). The embryo within the egg has its abdomen curved dorsalwards as amongst the Isopoda.
Cinipedia. The segmentation of Balanus and Lepas commences by the segregation of the constituents of the egg into a more protoplasmic portion, and a portion formed mainly of food material. The former separates from the latter as a distinct segment, and then divides into two not quite equal portions. The division of the protoplasmic part of the embryo continues, and the resulting segments grow round the single yolk segment. The point where they finally enclose it is situated on the ventral surface (Lang) at about the position of the mouth (?).
After being enclosed by the protoplasmic cells the yolk divides, and gives rise to a number of cells, which probably supply the material for the walls of the mesenteron. The external layer of protoplasm forms the so-called blastoderm, and soon (Arnold, Lang) becomes thickened on the dorsal surface.
The embryo is next divided by two constrictions into three segments ; and there are formed the three appendages corresponding to these, which are
at first simple. The two posterior soon become biramous. The larva leaves the egg before any further appendages become formed.
Comparative development of the organs.
Central nervous system. The ventral nerve cord of the Crustacea develops as a thickening of the epiblast along the median ventral line ; the differentiation of which commences in front, and thence extends backwards. The ventral cord is at first unsegmented. The supra-oesophageal ganglia originate as thickenings of the epiblast of the procephalic lobes.
The details of the above processes are still in most cases very imperfectly known. The fullest account we have is that of Reichenbach (No. 488) for Astacus. He finds that the supra- cesophageal ganglia and ventral cord arise as a continuous formation, and not independently as would seem to be the case in Chsetopoda. The supra-cesophageal ganglia are formed from the procephalic lobes. The first trace of them is visible in the form of a pair of pits, one on each side of the middle line. These pits become in the Nauplius stage very deep, and their walls are then continued into two ridges where the epiblast is several cells deep, which pass backwards one on each side of the mouth. The walls of the pits are believed by Reichenbach to give rise to the optic portions of the supra-cesophageal ganglia, and the epiblastic ridges to the remainder of the ganglia and to the circum-cesophageal commissures. At a much later stage, when the ambulatory feet have become formed, a median involution of epiblast in front of the mouth and between the two epiblast ridges gives rise to a central part of the supracesophageal ganglia. Five elements are thus believed by Reichenbach to be concerned in the formation of these ganglia, viz. two epiblast pits, two epiblast ridges, and an involution of epiblast between the latter. It should be noted however that the fate neither of the pair of pits, nor of the median involution, appears to have been satisfactorily worked out. The two epiblast ridges, which pass back from the supra-cesophageal ganglia on each side of the mouth, are continued as a pair of thickenings of the epiblast along the sides of a median ventral groove. This groove is deep in front and shallows out posteriorly. The thickenings on the sides of this groove no doubt give rise to the lateral halves of the ventral cord, and the cells of the groove itself are believed by Reichenbach, but it appears to me without sufficient evidence, to become invaginated also and to assist in forming the ventral cord. When the ventral cord becomes separated from the epiblast the two halves of it are united in the middle line, but it is markedly bilobed in section.
In the Isopoda it would appear both from Bobretzky's and Bullar's observations that the ventral nerve cord arises as an unpaired thickening of the epiblast in which there is no trace of anything like a median involution. After this thickening has become separated from the epiblast a slight
522 DEVELOPMENT OF ORGANS.
median furrow indicates its constitution out of two lateral cords. The supra-oesophageal ganglia are stated to be developed quite simply as a pair of thickenings of the procephalic lobes, but whether they are from the first continuous with the ventral cord does not appear to have been determined.
The later stages in the differentiation of the ventral cord are, so far as is known, very similar throughout the Crustacea. The ventral cord is, as has been stated, at first unsegmented (fig. 241 A, vg\ but soon becomes divided by a series of constrictions into as many ganglia as there are pairs of appendages or segments (fig. 241 B, vg).
There appears either on the ventral side (Oniscus) or in the centre (Astacus, Palaemon) of the two halves of each segment or ganglion a space filled with finely punctuated material, which is the commencement of the commissural portion of the cords. The commissural tissue soon becomes continuous through the length of the ventral cord, and is also prolonged into the supracesophageal ganglia.
After the formation of the commissural tissue the remaining cells of the cord form the true ganglion cells. A gradual separation of the ganglia next takes place, and the cells become confined to the ganglia, which are finally only connected by a double band of commissural tissue. The commissural tissue not only gives rise to the longitudinal cords connecting the successive ganglia, but also to the transverse commissures which unite the two halves of the individual ganglia.
The ganglia usually, if not always, appear at first to correspond in number with the segments, and the smaller number so often present in the adult is due to the coalescence of originally distinct ganglia.
Organs of special sense. Comparatively little is known on this head. The compound eyes are developed from the coalescence of two structures, both however epiblastic, viz. (i) part of the superficial epiblast of the procephalic lobes ; (2) part of the supra-cesophageal ganglia. The former gives rise to the corneal lenses, the crystalline cones, and the pigment surrounding them ; the latter to the rhabdoms and the cells which encircle them. Between these two parts a mesoblastic pigment is interposed.
Of the development of the auditory and olfactory organs almost nothing is known.
Dorsal organ. In a considerable number of the Malacostraca and Branchiopoda a peculiar organ is developed from the epiblast in the anterior dorsal region. This organ has been called the dorsal organ. It appears to be of a glandular nature, and is usually very large in the embryo or larva and disappears in the adult ; but in some Branchiopoda it persists through life. In most cases it is unpaired, but in some instances a paired organ appears to take its place.
Various views as to its nature have been put forward. There is but little doubt of its being glandular, and it is possible that it is a provisional renal organ, though so far as I know concretions have not yet been found in it.
Its development has been most fully studied in the Isopoda.
In Cymothoa (Bullar, No. 499) there appears on the dorsal surface, in the region which afterwards becomes the first thoracic segment, an unpaired linear thickening of the blastoderm. This soon becomes a circular patch, the central part of which is invaginated so as to communicate with the exterior by a narrow opening only (fig. 242). It becomes at the same time attached to the inner egg membrane. It retains this condition till the close of larval life.
In Oniscus (Dohrn, No. 500 ; Bobretzky, No. 498) there appears very early a dorsal patch of thickened cells. These cells become attached at their edge to the inner egg membrane and gradually separated from the embryo, with which they finally only re- , FlG - W- DIAGRAMMATIC SECTION OF . , ... CYMOTHOA SHEWING THE DORSAL ORGAN. main in connection by a hollow (F rom Bullar.)
column of cells (fig. 241 A, do).
The original patch now gradually spreads over the inner egg membrane, and forms a transverse saddle-shaped band of flattened cells which engirths the embryo on all but the ventral side.
In the Amphipods the epiblast cells remain attached for a small area on the dorsal surface to the first larval skin, when this is formed. This patch of cells, often spoken of as a micropyle apparatus, forms a dorsal organ equivalent to that in Oniscus. A perforation is formed in it at a later
DEVELOPMENT OF ORGANS.
period. A perhaps homologous structure is found in the embryos of Euphausia, Cuma, etc.
In many Branchiopoda a dorsal organ is found. Its development has been studied by Grobben in Moina. It persists in the adult in Branchipus, Limnadia, Estherea, etc.
In the Copepoda a dorsal organ is sometimes found in the embryo ; Grobben at any rate believes that he has detected an organ of this nature in the embryo of Cyclops serrulatus.
A paired organ which appears to be
FIG. 243. DIAGRAMMATIC SECTION OF AN EMBRYO OF ASELLUS AQUATICUS TO SHEW THE PAIRED DORSAL ORGAN. (From Bullar ; after E. van Beneden.)
of the same nature has been found in Asellus and Mysis.
In Asellus (Rathke (No. 501), Dohrn (No. 500), Van Beneden (No. 497)) this organ originates as two cellular masses at the sides of the body just behind the region of the procephalic lobes. Each of them becomes trifoliate and bends towards the ventral surface. In each of their lobes a cavity arises and finally the three cavities unite, forming a trilobed cavity open to the yolk. This organ eventually becomes so large that it breaks through the egg membranes and projects at the sides of the embryo (fig. 243\ Though formed before the appendages it does not attain its full development till considerably after the latter have become well established.
In Mysis it appears during the Nauplius stage as a pair of cavities lined by columnar cells, which atrophy very early.
Various attempts have been made to identify organs in other Arthropod embryos with the dorsal organ of the Crustacea, but the only organ at all similar which has so far been described is one found in the embryo of Linguatula (vide Chapter XIX.), but there is no reason to think that this organ is really homologous with the dorsal organ of the Crustacea.
The mesoblast. The mesoblast in the types so far investigated arises from the same cells as the hypoblast, and appears as a somewhat irregular layer between the epiblast and the hypoblast. It gives rise to the same parts as in other forms, but it is remarkable that it does not, in most Decapods and Isopods
(and so far we do not know about other forms), become divided into somites, at any rate with the same distinctness that is usual in Annelids and Arthropods. Not only so, but there is at first no marked division into a somatic and splanchnic layer with an intervening body cavity. Some of the cells become differentiated into the muscles of the body wall and limbs ; and other cells, usually in the form of a very thin layer, into the muscles of the alimentary tract. In the tail of Palcsmon Bobretzky noticed that the cells about to form the muscles of the body were imperfectly divided into cubical masses corresponding with the segments ; which however, in the absence of a central cavity, differed from typical mesoblastic somites. In Mysis Metschnikoff states that the mesoblast becomes broken up into distinct somites. Further investigations on this subject are required. The body cavity has the form of irregular blood sinuses amongst the internal organs.
Heart. The origin and development of the heart and vascular system are but very imperfectly known.
In Phyllopods (Branchipus) Claus (No. 454) has shewn that the heart is formed by the coalescence of the lateral parts of the mesoblast of the ventral plates. The chambers are formed successively as the segments to which they belong are established, and the anterior chambers are in full activity while the posterior are not yet formed.
In Astacus and Palaemon, Bobretzky finds that at the stage before the heart definitely appears there may be seen a solid mass of mesoblast cells in the position which it eventually occupies 1 ; and considers it probable that the heart originates from this mass. At the time when the heart can first be made out and before it has begun to beat, it has the form of an oval sack with delicate walls separated from the mesenteron by a layer of splanchnic mesoblast. Its cavity is filled with a peculiar plasma which also fills up the various cavities in the mesoblast. Around it a pericardial sack is soon formed, and the walls of the heart become greatly thickened. Four bands pass off from the heart, two dorsalwards which become fixed to the integument, and two ventralwards. There is also a median band of cells connecting the heart with the dorsal integument. The main arteries arise as direct prolongations of the heart. Dohrn's observations on Asellus greatly strengthen the view that the heart originates from a solid mesoblastic mass, in that he was able to observe the hollowing out of the mass in
1 Reichenbach describes these cells, and states that there is a thickening of the epiblast adjoining them. In one place he states that the heart arises from this thickening of epiblast, and in another that it arises from the mesoblast. An epiblastic origin of the heart is extremely improbable.
526 DEVELOPMENT OF ORGANS.
the living embryo (cf. the development of the heart in Spiders). Some of the central cells (nuclei, Dohrn) become blood corpuscles. The formation of these is not, according to Dohrn, confined to the heart, but takes place in situ in all the parts of the body (antennae, appendages, etc.). The corpuscles are formed as free nuclei and are primarily derived from the yolk, which at first freely communicates with the cavities of the appendages.
Alimentary tract. In Astacus the formation of the mesenteron by invagination, and the absorption of the yolk by the hypoblast cells, have already been described. On the absorption of the yolk the mesenteron has the form of a sack, the walls of which are formed of immensely long cells the yolk pyramids at the base of which the nucleus is placed (fig. 238 B). This sack gives rise both to the portion of the alimentary canal between the abdomen and the stomach and to the liver. The epithelial wall of both of these parts is formed by the outermost portions of the pyramids with the nuclei and protoplasm becoming separated off from the yolk as a layer of flat epithelial cells. The yolk then breaks up and forms a mass of nutritive material filling up the cavity of the mesenteron.
The differentiation both of the liver and alimentary tract proper first takes place on the ventral side, and commences close to the point where the proctodasum ends, and extends forward from this point. A layer of epithelial cells is thus formed on the ventral side of the mesenteron which very soon becomes raised into a series of longitudinal folds, one of which in the middle line is very conspicuous. The median fold eventually, by uniting with a corresponding fold on the dorsal side, gives rise to the true mesenteron ; while the lateral folds form parallel hepatic cylinders, which in front are not constricted off from the alimentary tract. The lateral parts of the dorsal side of the mesenteron similarly give rise to hepatic cylinders. The yolk pyramids of the anterior part of the mesenteron, which projects forwards as a pair of diverticula on each side to the level of the stomach, are not converted into hepatic cylinders till after the larva is hatched.
The proctodasum very early opens into the mesenteron, but the stomodaeum remains closed till the differentiation of the mid-gut is nearly completed. The proctodaeum gives rise to the abdominal part of the intestine, and the stomodaeum to the oesophagus and stomach. The commencement of the masticatory apparatus in the latter appears very early as a dorsal thickening of the epithelium.
The primitive mesenteron in Palaemon differentiates itself into the permanent mid-gut and liver in a manner generally similar to that in Astacus, though the process is considerably less complicated. A distinct layer of cells separates itself from the outer part of the yolk pyramids, and gives rise to the glandular lining both of the mid-gut and of the liver. The differentiation of this layer commences behind, and the mid-gut very soon communicates freely with the proctodasum. The lateral parts of the primitive mesenteron become constricted into four wings, two directed forwards and two backwards ; these, after the yolk in them has become absorbed, constitute the liver. The median part simply becomes the me
senteron. The stomachic end of the stomodaeum lies in contact with the mesenteron close to the point where it is continued into the hepatic diverticula, and, though the partition-wall between the two becomes early very thin, a free communication is not established till the yolk has been completely absorbed.
The alimentary tract in the Isopoda is mainly if not entirely formed from the proctodaeum and stomodaeum, both of which arise before any other part of the alimentary system as epiblastic invaginations, and gradually grow inwards (fig. 244). In Oniscus the liver is formed as two discs at the surface of the yolk on each side of the anterior part of the body. Their walls are composed of cubical cells derived from the yolk cells, the
s r " a qcaggaw. rt -j_ .-. f .i~T' : . -^a^Mi^ . - .. >va^^^
FlG. 244. TWO LONGITUDINAL SECTIONS THROUGH THE EMBRYO OF ONISCUS
MURARIUS. (After Bobretzky.)
st. stomodaeum ; pr. proctodseum ; hy. hypoblast formed of large nucleated cells imbedded in yolk ; m. mesoblast ; vg. ventral nerve cord ; jr^. supra- oesophageal ganglion ; li. liver; do. dorsal organ; zp. rudiment of masticatory apparatus.
origin of which was spoken of on p. 516. These two discs gradually take the form of sacks (fig. 244 B, li.) freely open on their inner side to the yolk. As these sacks continue to grow the stomodaeum and proctodaeum do not remain passive. The stomodaeum, which gives rise to the oesophagus and stomach of the adult, soon exhibits a posterior dilatation destined to become the stomach, on the dorsal wall of which a well-marked prominence the earliest trace of the future armature is soon formed (fig. 244 B, xp}. The proctodaeum (pr) grows with much greater rapidity than the stomodaeum, and its end adjoining the yolk becomes extremely thin or even broken through. In the earliest stages it was surrounded by the yolk cells, but in its later growth the yolk cells become gradually reduced in number and appear to recede before it so much so that one is led to conclude that the later growth of the proctodaeum takes place at the expense of the yolk cells.
The liver sacks become filled with a granular material without a trace of cells ; their posterior wall is continuous with the yolk cells, and their anterior lies close behind the stomach. The proctodaeum continually grows forwards till it approaches close to the stomodaeum, and the two
528 DEVELOPMENT OF ORGANS.
liver sacks, now united into one at their base, become directly continuous with the proctodaeum. By the stage when this junction is effected the yolk cells have completely disappeared. It seems then that in Oniscus the yolk cells (hypoblast) are mainly employed in giving rise to the walls of the liver ; but that they probably also supply the material for the later growth of the apparent proctodaeum. It becomes therefore necessary to conclude that the latter, which might seem, together with the stomodasum, to form the whole alimentary tract, does in reality correspond to the proctodaeum and mesenteron together, though the digestive fluids are no doubt mainly secreted not in the mesenteron but in the hepatic diverticula. The proctodaeum and stomodaeum at first meet each other without communicating, but before long the partition between the two is broken through.
In Cymothoa (Bullar, No. 499) the proctodaeum and stomodaeum develop in the same manner as in Oniscus, but the hypoblast has quite a different form. The main mass of the yolk, which is much greater than in Oniscus, is not contained in definite yolk cells, but the hypoblast is represented by (i) two solid masses of cells, derived apparently from the inner layer of blastoderm cells, which give rise to the liver ; and (2) by a membrane enclosing the yolk in which nuclei are present.
The two hepatic masses lie on the surface of the yolk, and each of them becomes divided into three short caecal tubes freely open to the yolk. The stomodaeum soon reaches its full length, but the proctodaeum grows forwards above the yolk till it meets the stomodaeum. By the time this takes place the liver caeca have grown into three large tubes filled with fluid, and provided with a muscular wall. They now lie above the yolk, and no longer communicate directly with the cavity of the yolk sack, but open together with the yolk sack into the point of junction of the proctodaeum and stomodaeum. The yolk sack of Cymothoa no doubt represents part of the mesenteron, but there is no evidence in favour of any part of the apparent proctodaeum representing it also, though it is quite possible that it may do so. The relations of the yolk sack and hepatic diverticula in Cymothoa appear to hold good for Asellus and probably for most Isopoda.
The differences between the Decapods and Isopods in the development of the mesenteron are not inconsiderable, but they are probably to be explained by the relatively larger amount of food yolk in the latter forms. The solid yolk in the Isopods on this view represents the primitive mesenteron of Decapods after the yolk has been absorbed by the hypoblast cells. Starting from this standpoint we find that in both groups the lateral parts of the mesenteron become the liver. In Decapods the middle part becomes directly converted into the mid-gut, the differentiation of it commencing behind and proceeding forwards. In the Isopods, owing to the mesenteron not having a distinct cavity, the differentiation of it, which proceeds forwards as in Decapods, appears simply like a prolongation forwards of the proctoda?um, the cells for the prolongation being probably supplied from the yolk. In Cymothoa the food yolk is so bulky that a special yolk sack is developed
for its retention, which is not completely absorbed till some time after the alimentary canal has the form of a continuous tube. The walls of this yolk sack are morphologically a specially developed part of the mesenteron.
(447) C. Spence Bate. " Report on the present state of our knowledge of the Crustacea." Report of the British Association for 1878.
(448) C. Claus. Untersuchungen zur Erforschung der genealogischen Grundlage des Crustaceen- Systems. Wien, 1876.
(449) A. Dohrn. "Geschichte des Krebsstammes. " Jenaische Zeitschrift, Vol. VI. 1871.
(450) A. Gerstaecker. Bronris Thierreich, Bd. v. Arthropoda, 1866.
(451) Th. H. Huxley. The Anatomy of Invertebrated Animals. London, 1877.
(452) Fritz Mliller. Fur Darwin, 1864. Translation, Facts for Darwin. London, 1869.
(453) Brauer. "Vorlaufige Mittheilung iiber die Entwicklung u. Lebensweise des Lepidurus (Apus) productus." Sitz. der Ak. d. Wiss. Wien, Vol. LXIX., 1874.
(454) C. Claus. "Zur Kenntniss d. Baues u. d. Entwicklung von Branchipus stagnalisu. Apus cancriformis." Abh. d. kb'nig. Gesell. der Wiss. Gb'ttingen, Vol. XVIII. 1873.
(455) C. Grobben. "Zur Entwicklungsgeschichte d. Moina rectirostris." Arbeit, a. d. zoologisch. Institute Wien, Vol. II., 1879.
(456) E. Grube. " Bemerkungen uber die Phyllopoden nebst einer Uebersicht etc." Archivf. Naturgeschichte, Vol. xix., 1853.
(457) N. Joly. " Histoire d'un petit Crustace (Artemia salina, Leach} etc." Annales d. Sciences Natur., 2nd ser., Vol. xiii., 1840.
(458) N. Joly. " Recherches zoologiques anatomiques et physiologiques sur 1'Isaura cycladoides ( = Estheria) nouveau genre, etc." Annales d. Sciences Nat., 2nd ser., Vol. xvii., 1842.
(459) Lereboullet. " Observations sur la generation et le developpement de la Ltmnadia de Hermann." Annales d. Sciences Natur., <$th ser., Vol. v., 1866.
(460) F. Leydig. " Ueber Artemia salina u. Branchipus stagnalis." Zeit. f. wiss. ZooL, Vol. in., 1851.
(461) G. O. Sars. " Om en dimorph Udvikling samt Generationsvexel hos Leptodora." Vidensk. Selskab. Forhand, 1873.
(462) G. Zaddach. De apodis cancreformis Schaeff. anatome et historia evolutionis. Dissertatio inanguralis zootomica. Bonnse, 1841.
(463) C. Claus. " Ueber den Bau u. die systematische Stellung von Nebalia." Zeit.f. wiss. Zool., Bd. xxn. 1872.
(464) E. Metschnikoff. Development of Nebalia (Russian), 1868.
B. II. 34
(465) E. van Beneden, " Recherches sur 1'Embryogenie des Crustaces. n. DeVeloppement des Mysis." Bullet, de rAcadtmie roy. de Belgique, second series, Tom. xxvin. 1869.
(46G) C. Glaus. " Ueber einige Schizopoden u. niedere Malakostraken." Zett. f. wiss. Zoologie, Bd. XII I., 1863.
(467) A. Dohrn. " Untersuchungen Ub. Bau u. Entwicklung d. Arthropoden." Zeit.f. wiss. Zool.y Bd. XXL, 1871, .p. 375. Peneus zoaea (larva of Euphausia).
(468) E. Metschnikoff. " Ueber ein Larvenstadium von Euphausia." Zeit. fiir wiss. Zool., Bd. xix., 1869.
(469) E. Metschnikoff. " Ueber den Naupliuszustand von Euphausia. " Zeit. fiir wiss. Zool., Bd. XXI., 1871.
(470) S pence Bate. "On the development of Decapod Crustacea." Phil. Trans., 1858.
(471) Spence Bate. " On the development of Pagurus." Ann. and Mag. Nat. History, Series 4, Vol. II., 1868.
(472) N. Bobretzky. Development of Astacus and Palamon. Kiew, 1873. (Russian.)
(473) C. Glaus. "Zur Kenntniss d. Malakostrakenlarven. " Wiirzb. naturw. Zeitschrift, 1861.
(474) R. Q. Couch. "On the Metamorphosis of the Decapod Crustaceans." Report Cornwall Polyt. Society. 1848.
(475) Du Cane. "On the Metamorphosis of Crustacea." Ann. and Mag. of Nat. History, 1839.
(476) Walter Faxon. " On the development of Palsemonetes vulgaris." Bull, of the Mus. of Camp. Anat. Harvard, Cambridge, Mass., Vol. v., 1879.
(477) A. Dohrn. " Untersuchungen lib. Bau u. Entwicklung d. Arthropoden." " Zur Entwicklungsgeschichte der Panzerkrebse. Scyllarus Palinurus." Zeit. f. wiss. Zool., Bd. xx., 1870.
(478) A. Dohrn. "Untersuchungen lib. Bau u. Entwicklung d. Arthropoden. Erster Beitrag z. Kenntniss d. Malacostraken u. ihrer Larven Amphion Reynaudi, Lophogaster, Portunus, Porcellanus, Elaphocaris. " Zeit. f. wiss. Zool., Bd. xx., 1870.
(479) A. Dohrn. "Untersuchungen lib. Bau u. Entwicklung d. Arthropoden. Zweiter Beitrag, etc." Zeit.f. wiss. Zool., Bd. xxi., 1871.
(480) N. Joly. " Sur la Caridina Desmarestii." Ann. Scien. Nat., Tom. xix., 1843.
(481) Lereboullet. " Recherches d . 1'embryologie comparee sur le developpement du Brochet, de la Perche et de 1'Ecrevisse." Mem. Savans ktrang. Paris, Vol. xvn., 1862.
(482) P. Mayer. "Zur Entwicklungsgeschichte d. Dekapoden." Jenaische Zeitschrift, Vol. XI., 1877.
(483) F r i t z M u 1 1 e r. " Die Verwandlung der Porcellana." Archivf. Natnrgeschichte, 1862.
(484) Fritz Muller. " Die Verwandlungen d. Garneelen," Archiv f. Naturgesch., Tom. xxix.
(485) Fritz Muller. " Ueber die Naupliusbrut d. Garneelen." Zeit f. wiss. Zool., Bd. xxx., 1878.
(486) T. J. Parker. "An account of Reichenbach's researches on the early development of the Fresh-water Crayfish." Quart. J. of M. Science, Vol. xvin., 1878.
(487) H. Rathke. Ueber die Bildung u. Entivicklung d. Flusskrebses. Leipzig, 1829.
(488) H. Reichenbach. " Die Embryoanlage u. erste Entwicklung d. Flusskrebses." Zeit.f. wiss. Zool., Vol. xxix., 1877.
(489) F. Richters. " Ein Beitrag zur Entwicklungsgeschichte d. Loricaten." Zeit.f. wiss. Zool., Bd. xxiil., 1873.
(490) G. O. Sars. " Om Hummers posiembryonale Udvikling. " Vidensk Selsk. Fork. Christiania, 1874.
(491) Sidney J. Smith. " The early stages of the American Lobster. " Trans, of the Connecticut Acad. of Arts and Sciences, Vol. n., Part 2, 1873.
(492) R. v. Willemoes Suhm. " Preliminary note on the development of some pelagic Decapoda." Proc. of Royal Society, 1876.
(493) W. K. Brooks. " On the larval stages of Squilla empusa." Chesapeake Zoological Laboratory, Scientific results of the Session of 1878. Baltimore, 1879 (494) C. Claus. "Die Metamorphose der Squilliden." Abhand. der kbnigl. Gesell. der Wiss. zu Gbttingen, 1871.
(495) Fr. Muller. " Bruchstuck a. der Entwicklungsgeschichte d. Maulfusser I. und II." Archiv f. Naturgeschichte, Vol. xxvin., 1862, and Vol. xxix., 1863.
(496) A. Dohrn. " Ueber den Bau u. Entwicklung d. Cumaceen." Jenaische Zeitschrift, Vol. v., 1870.
(497) Ed. van Beneden. " Recherches sur 1'Embryogenie des Crustaces. I. Asellus aquaticus." Bull, de FAcad. roy Belgique, 2me serie, Tom. xxvni., No. 7, 1869.
(498) N. Bobretzky. " Zur Embryologie des Oniscus murarius." Zeit. fur wiss. Zool., Bd. xxiv., 1874.
(499) J. F. Bullar. "On the development of the parasitic Isopoda." Phil. Trans., Part II., 1878.
(500) A. Dohrn. " Die embryonale Entwicklung des Asellus aquaticus." Zeit. f. wiss. Zool., Vol. xvn., 1867.
(501) H. Rathke. Untersuchungen iiber die Bildung tmd Entwicklung der Wasser-Assel. Leipzig, 1832.
(502) H. Rathke. Zur Morphologic. Reisebemerkungen aus Taurien. Riga u. Leipzig, 1837. (Bopyrus, Idothea, Ligia, lanira.)
(503) Ed. van Beneden and E. Bessels. "M&noire sur la formation du blastoderme chez les Amphipodes, les Lerneens et les Cope"podes." Classe des Sciences deTAcad. roy. de Belgique, Vol. xxxiv., 1868.
(504) De la Valletta St George. " Studien iiber die Entwicklung der Amphipoden." Abhand. d. naturfor. Gesell. zu Halle, Bd. v., 1860.
(505) E. van Beneden and E. Bessels. " Me*moire sur la formation du blastoderme chez les Amphipodes, les Lerndens et Copepodes." Classe des Sciences de FAcad. roy. de Belgique, Vol. xxxiv., 1868.
(506) E. van Beneden. " Recherches sur 1'Embryogenie des Crustaces iv. Anchorella, Lerneopoda, Branchiella, Hessia." Bull, de FAcad. roy. de Belgique, 2me serie, T. xxix., 1870.
(507) C. Claus. Zur Anatomie u. Entwicklungsgeschichte d. Copepoden.
(508) C. Claus. " Untersuchungen Uber die Organisation u. Verwandschaft d. Copepoden." Wiirzburger naturwiss. Zeitschrift, Bd. III., 1862.
(509) C. Claus. " Ueber den Bau u. d. Entwicklung von Achtheres percarum." Zeit.f. wiss. Zool., Bd. XL, 1862.
(510) C. Claus. Die freilebenden Copepoden mit besonderer Berucksichtigung der Fauna Deutschlands, des Nordsee u. des Mittelmeeres. Leipzig, 1863.
(511) C. Claus. " Ueber d. Entwicklung, Organisation u. systematische Stellung d. Argulidse." Zeit.f. wiss. Zool., Bd. xxv., 1875.
(512) P. P. C. Hoek. " Zur Entwicklungsgeschichte d. Entomostracen." Niederldndisches Archiv, Vol. IV., 1877.
(513) N o r d m a n n. Mikrographische Beitrdge zur Naturgeschichte der ivirbellosen l^hiere. Zweites Heft. 1832.
(514) Salensky. " Sphseronella Leuckartii." Archivf. Naturgeschichte, 1868.
(515) F. Vejdovsky. "Untersuchungen Ub. d. Anat. u. Metamorph. v. Tracheliastes polycolpus." Zeit.f. wiss. Zool., Vol. xxix., 1877.
(516) C. Spence Bate. "On the development of the Cirripedia." Annals and Mag. of Natur. History. Second Series, Vin., 1851.
(517) E. van Beneden. " DeVeloppement des Sacculines." Bull, de I" Acad. roy. de Belg., 1870.
(518) C. Claus. Die Cypris-dhnliche Larve der Cifripedien. Marburg, 1869.
(519) Ch. Darwin. A monograph of the sub-class Cirripedia, i Vols., Ray Society, 18514.
(520) A. Dohrn. ' Untersuchungen iiber Bau u. Entwicklung d. Arthropoden ix. Eine neue Naupliusform (Archizoea gigas)." Zeit. f. wiss. Zool., Bd. xx., 1870.
(521) P. P. C. Hoek. "Zur Entwicklungsgeschichte der Entomostraken i. Kinbryologie von Balanus." Niederldndisches Archiv fur Zoologie, Vol. III., 1876 7.
(522) R. Kossmann. "Suctoria u. Lepadidoc." Arbeiten a. d. zool.-zoot. Instituted. Univer. Wiirz., Vol. I., 1873.
(523) Aug. Krohn. " Beobachtungen iiber die Entwicklung der Cirripedien." Wiegmanris Archiv fur Naturgesch., xxvi., 1860.
(524) E. Metschnikoff. Sitzungsberichte d. Versammlung deutscher Naturforscher zu Hannover, 1865. (Balanus balanoides.)
(525) Fritz Muller. "Die Rhizocephalen." Archiv f. Naturgeschichte, 1862-3.
(526) F. C. Noll. " Kochlorine hamata, ein bohrendes Cirriped." Zeit.f. wiss. Zool., Bd. xxv., 1875.
(527) A. Pagenstecher. " Beitrage zur Anatomic und Entwicklungsgeschichte von Lepas pectinata." Zeit.f. wiss. ZooL, Vol. xni., 1863.
(528) J. V. Thompson. Zoological Researches and Illustrations, Vol. I., Part I. Memoir IV. On the Cirripedes or Barnacles. 8vo. Cork, 1830.
(529) J. V. Thompson. " Discovery of the Metamorphosis in the second type of the Cirripedes, viz. the Lepades completing the natural history of these singular animals, and confirming their affinity with the Crustacea." Phil. Trans. 1835. Part n.
(530) R. von Willemoes Suhm. "On the development of Lepas fascicularis." Phil. Trans., Vol. 166, 1876.
(531) C. Glaus. " Zur naheren Kenntniss der Jugendformen von Cypris ovum." Zeit.f. wiss. ZooL, Bd. xv., 1865.
(532) C. Glaus. "Beitrage zur Kenntniss d. Ostracoden. Entwicklungsgeschichte von Cypris ovum." Schriften d. Gesell. zur Befdrderung d. gesamm. Naturwiss. zu Marburg, Vol. IX., 1868.
PCECILOPODA, PYCNOGONIDA, TARDIGRADA, AND LINGUATULIDA; AND COMPARATIVE SUMMARY OF ARTHROPODAN DEVELOPMENT.
THE groups dealt with in the present Chapter undoubtedly belong to the Arthropoda. They are not closely related, and in the case of each group it is still uncertain with which of the main phyla they should be united. It is possible that they may all be offshoots from the Arachnidan phylum.
The development of Limulus has been studied by Dohrn (No. 533) and Packard (No. 534). The ova are laid in the sand near the spring-tide marks. They are enveloped in a thick chorion formed of several layers ; and (during the later stages of development at any rate) there is a membrane within the chorion which exhibits clear indications of cell outlines 1 .
There is a centrolecithal segmentation, which ends in the formation of a blastoderm enclosing a central yolk mass. A ventral plate is then formed, which is thicker in the region where the abdomen is eventually developed. Six segments soon become faintly indicated in the cephalothoracic region, the ends of which grow out into prominent appendages (fig. 245 A) ; of these there are six pairs, which increase in size from before backwards. A stomodaeum (m) is by this time established and is placed well in front of the foremost pair of appendages'*-.
In the course of the next few days the two first appendages of the abdominal region become formed (vide fig. 245 C shewing those abdominal appendages at a later stage), and have a very different shape and direction to those of the cephalothorax. The appendages of the latter become
1 The nature of the inner membrane is obscure. It is believed by Packard to be moulted after the formation of the limbs, and to be equivalent to the amnion of Insects, while by Dohrn it is regarded as a product of the follicle cells.
2 Dohrn finds at first only five appendages, but thinks that the sixth (the anterior one) may have been present but invisible.
flexed in the middle in such a way that their ends become directed towards the median line (fig. 245 B). The body of the embryo (fig. 245 B) is now distinctly divided into two regions the cephalothoracic in front, and the abdominal behind, both divided into segments.
FIG. 245. THREE STAGES IN THE DEVELOPMENT OF LIMULUS POLYPHEMUS. (Somewhat modified from Packard.)
A. Embryo in which the thoracic limbs and mouth have become developed on the ventral plate. The outer line represents what Packard believes to be the amnion.
B. Later embryo from the ventral surface.
C. Later embryo, just before the splitting of the chorion from the side. The full number of segments of the abdomen, and three abdominal appendages, have become established ; m. mouth ; I IX. appendages.
Round the edge of the ventral plate there is a distinct ridge the rudiment of the cephalothoracic shield.
With the further growth of the embryo the chorion becomes split and cast off, the embryo being left enclosed within the inner membrane. The embryo has a decided ventral flexure, and the abdominal region grows greatly and forms a kind of cap at the hinder end, while its vaulted dorsal side becomes divided into segments (fig. 245 C). Of these there are according to Dohrn seven, but according to Packard nine, of which the last forms the rudiment of the caudal spine.
In the thoracic region the nervous system is by this stage formed as a ganglionated cord (Dohrn), with no resemblance to the peculiar cesophageal ring of the adult. The mouth is stated by Dohrn to lie between the second pair of limbs, so that, if the descriptions we have are correct, it must have by this stage changed its position with reference to the appendages. Between the thorax and abdomen two papillae have arisen which form the
so-called lower lip of the adult, but from their position and late development they can hardly be regarded as segmental appendages. In the course of further changes all the parts become more distinct, while the membrane in which the larva is placed becomes enormously distended (fig. 246 A). The rudiments of the compound eyes are formed on the third (Packard) or fourth (Dohrn) segment of the cephalothorax, and the simple eyes near the median line in front. The rudiments of the inner process of the chelae of the cephalothoracic appendages arise as buds. The abdominal appendages become more plate-like, and the rudiments of a third pair appear behind the two already present. The heart appears on the dorsal surface.
An ecdysis now takes place, and in the stage following the limbs have approached far more closely to their adult state (fig. 246 A). The cephalothoracic appendages become fully jointed ; the two anterior abdominal appendages (vn.) have approached, and begin to resemble the oper
FlO. 246. TWO STAGES IN THE DEVELOPMENT OF LlMULUS POLYPHEMUS.
A. An advanced embryo enveloped in the distended inner membrane shortly before hatching ; from the ventral side.
B. A later embryo at the Trilobite stage, from the dorsal side. I., vii., VIII. First, seventh, and eight appendages.
cs. caudal spine ; se. simple eye ; ce. compound eye.
culum of the adult, and on the second pair is formed a small inner ramus. The segmentation of the now vaulted cephalothorax becomes less obvious, though still indicated by the arrangement of the yolk masses which form the future hepatic diverticula.
Shortly after this stage the embryo is hatched, and at about the time of hatching acquires a form (fig. 246 B) in which it bears, as pointed out by Dohrn and Packard, the most striking resemblance to a Trilobite.
Viewed from the dorsal surface (fig. 246 B) it is divided into two distinct regions, the cephalothoracic in front and the abdominal behind. The cephalothoracic has become much flatter and wider, has lost all trace of its previous segmentation, and has become distinctly trilobed. The
central lobe forms a well-marked keel, and at the line of insertion of the rim-like edge of the lateral lobes are placed the two pairs of eyes (se and ce). The abdominal region is also distinctly trilobed and divided into nine segments ; the last, which is merely formed of a median process, being the rudiment of the caudal spine. The edges of the second to the seventh are armed with a spine. The changes in the appendages are not very considerable. The anterior pair nearly meet in the middle line in front or the mouth ; and the latter structure is completely covered by an upper lip. Each abdominal appendage of the second pair is provided with four gill-lamellas, attached close to its base.
Three weeks after hatching an ecdysis takes place, and the larva passes from a trilobite into a limuloid form. The segmentation of the abdomen has become much less obvious, and this part of the embryo closely resembles its permanent form. The caudal spine is longer, but is still relatively short. A fourth pair of abdominal appendages is established, and the first pair have partially coalesced, while the second and third pairs have become jointed, their outer ramus containing four and their inner three joints. Additional gill-lamellae attached to the two basal joints of the second and third abdominal appendages have appeared.
The further changes are not of great importance. They are effected in a series of successive moults. The young larvae swim actively at the surface.
Our, in many respects, imperfect knowledge of the development of Limulus is not sufficient to shew whether it is more closely related to the Crustacea or to the Arachnida, or is an independent phylum.
The somewhat Crustacean character of biramous abdominal feet, etc. is not to be denied, but at the same time the characters of the embryo appear to me to be decidedly more arachnidan than crustacean. The embryo, when the appendages are first formed, has a decidedly arachnidan facies. It will be remembered that when the limbs are first formed they are all post-oral. They resemble in this respect the limbs of the Arachnida, and it seems to be probable that the anterior pair is equivalent to the cheliceras of Arachnida, which, as shewn in a previous section, are really post-oral appendages in no way homologous with antennae 1 .
The six thoracic appendages may thus be compared with the six Arachnidan appendages; which they resemble in their relation to the mouth, their basal cutting blades, etc.
The existence of abdominal appendages behind the six cephalothoracic does not militate against the Arachnidan affinities of Limulus, because in the Arachnida rudimentary abdominal appendages are always present in the embryo. The character of the abdominal appendages is probably
1 Dohrn believes that he has succeeded in shewing that the first pair of appendages of Limulus is innervated in the embryo from the supra-cesophageal ganglia. His observations do not appear to me conclusive, and, arguing from what we know of the development of the Arachnida, the innervation of these appendages in the adult can be of no morphological importance.
secondarily adapted to an aquatic respiration, since it is likely (for the reasons already mentioned in connection with the Tracheata) that if Limulus has any affinities with the stock of the Tracheata it is descended from airbreathing forms, and has acquired its aquatic mode of respiration. The anastomosis of the two halves of the generative glands is an Arachnidan character, and the position of the generative openings in Limulus is more like that in the Scorpion than in Crustacea.
A fuller study of the development would be very likely to throw further light on the affinities of Limulus, and if Packard's view about the nature of the inner egg membrane were to be confirmed, strong evidence would thereby be produced in favour of the Arachnidan affinities.
(533) A. Dohrn. "Untersuch. Ub. Bau u. Entwick. d. Arthropoden (Limulus polyphemus)." Jenaische Zeitschrift, Vol. vi., 1871.
(534) A. S. Packard. "The development of Limulus polyphemus." Mem. Boston Soc. Nat. History, Vol. II., 1872.
The embryos, during the first phases of their development, are always carried by the male in sacks which are attached to a pair of appendages (the third) specially formed for this purpose. The segmentation of the ovum is complete, and there is in most forms developed within the eggshell a larva with three pairs of two-jointed appendages, and a rostrum placed between the front pair.
It will be convenient to take Achelia kevis, studied by Dohrn (No. 536), as type.
The larva of Achelia when hatched is provided with the typical three pairs of appendages. The foremost of them is chelate, and the two following pairs are each provided with a claw. Of the three pairs of larvalappendages Dohrn states that he has satisfied himself that the anterior is innervated by the supra-cesophageal ganglion, and the two posterior by separate nerves coming from two imperfectly united ventral ganglia. The larva is provided with a median eye formed of two coalesced pigment spots, and with a simple stomach.
The gradual conversion of the larva into the adult takes place by the elongation of the posterior end of the body into a papilla, and the formation there, at a later period, of the anus ; while at the two sides of the anal papilla rudiments of a fresh pair of appendages the first pair of ambulatory limbs of the adult make their appearance. The three remaining pairs of limbs become formed successively as lateral outgrowths, and their development is accomplished in a number of successive ecdyses. As they are formed caeca from the stomach become prolonged into them. For each of them there appears a special ganglion. While the above changes are taking place the three pairs of larval appendages undergo considerable reduction. The anterior pair singly becomes smaller, the second loses its claw, and the third becomes reduced to a mere stump. In the adult the
second pair of appendages becomes enlarged again and forms the so-called palpi, while the third pair develops in the male into the egg-carrying appendages, but is aborted in the female. The first pair form appendages lying parallel to the rostrum, which are sometimes called pedipalpi and sometimes antennae.
The anal papilla is a rudimentary abdomen, and, as Dohrn has shewn, contains rudiments of two pairs of ganglia.
The larvae of Phoxichilidium are parasitic in various Hydrozoa (Hydractinia, etc.). After hatching they crawl into the Hydractinia stock. They are at first provided with the three normal pairs of larval appendages. The two hinder of these are soon thrown off, and the posterior part of the trunk, with the four ambulatory appendages belonging to it, becomes gradually developed in a series of moults. The legs, with the exception of the hindermost pair, are fully formed at the first ecdysis after the larva has become free. In the genus Pallene the metamorphosis is abbreviated, and the' young are hatched with the full complement of appendages.
The position of the Pycnogonida is not as yet satisfactorily settled. The six-legged larva has none of the characteristic features of the Nauplius, except the possession of the same number of appendages.
The number of appendages (7) of the Pycnogonida does not coincide with that of the Arachnida. On the other hand, the presence of chelate appendages innervated in the adult by the supra-cesophageal ganglia rather points to a common phylum for the Pycnogonida and Arachnida ; though as shewn above (p. 455) all the appendages in the embryo of true Arachnida are innervated by post-oral ganglia. The innervation of these appendages in . the larvae of Pycnogonida requires further investigation. Against such a relationship the extra pair of appendages in the Pycnogonida is no argument, since the embryos of most Arachnida are provided with four such extra pairs. The two groups must no doubt have diverged very early.
(535) G. Cavanna. " Studie e ricerche sui Picnogonidi." Pubblicazioni del R. Institute di Studi stiperiori in Firenze, 1877.
(536) An. Dohrn. " Ueber Entwickhuig u. Baud. Pycnogoniden." Jenaische Zeitschrift, Vol. v. 1870, and " Neue Untersuchungen lib. Pycnogoniden." Mitthdl. a. d. zoologischen Station zu Neafel, Bd. I. 1878.
(537) G. Hodge. " Observations on a species of Pycnogon, etc." Annal. and Mag. of Nat. Hist. Vol. ix. 1862.
(538) C. Semper. " Ueber Pycnogoniden u. ihre in Hydroiden schmarotzenden Larvenformen." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. I. 1874.
The development and metamorphosis of Pentastomum taenoides have been thoroughly worked out by Leuckart (No. 540) and will serve as type for the group.
In the sexual state it inhabits the nasal cavities of the dog. The early embryonic development takes place as the ovum gradually passes down the uterus. The segmentation appears to be complete ; and gives rise to an oval mass in which the separate cells can hardly be distinguished. This gradually differentiates itself into a characteristic embryo, divided into a tail and trunk. The tail is applied to the ventral surface of the trunk, and on the latter two pairs of stump-like unsegmented appendages arise, each provided with a pair of claws. At the anterior extremity of the body is formed the mouth, with a ventral spine and lateral hook, which are perhaps degenerated jaws. The spine functions as a boring apparatus, and an apparatus with a similar function is formed at the end of the tail. A larval cuticle now appears, which soon becomes detached from the embryo, except on the dorsal surface, where it remains firmly united to a peculiar papilla. This papilla becomes eventually divided into two parts, one of which remains attached to the cuticle, while the part connected with the embryo forms a raised cross placed in a cup- shaped groove. The whole structure has been compared, on insufficient grounds, to the dorsal organ of the Crustacea.
The eggs, containing the embryo in the condition above described, are eventually carried out with the nasal slime, and, if transported thence into the alimentary cavity of a rabbit or hare, the embryos become hatched by the action of the gastric juice. From the alimentary tract of their new host they make their way into the lungs or liver. They here become enveloped in a cyst, in the interior of which they undergo a very remarkable metamorphosis. They are, however, so minute and delicate that Leuckart was unable to elucidate their structure till eight weeks after they had been swallowed. At this period they are irregularly-shaped organisms, with a most distant resemblance to the earlier embryos. They are without their previous appendages, but the alimentary tract is now distinctly differentiated. The remains of two cuticles in the cyst seem to shew that the above changes are effected in two ecdyses.
In the course of a series of ecdyses the various organs of the larval form known as Pentastomum denticulatum continue to become differentiated. After the first (= third) ecdysis the cesophageal nerve-ring and sexually undifferentiated generative organs are developed. At the fourth (=sixth) ecdysis the two pairs of hooks of the adult are formed in pockets which appeared at a somewhat earlier stage ; and the body acquires an annulated character. At a somewhat earlier period rudiments of the external generative organs indicate the sex of the larva.
After a number of further ecdyses, which are completed in about six months after the introduction of the embryos into the intermediate host, the larva attains its full development, and acquires a form in which it has long been known as Pentastomum denticulatum. It now leaves its cyst and begins to move about. It is in a state fit to be introduced into its final host ; but if it be not so introduced it may become encysted afresh.
If the part of a rabbit or hare infected by a Pentastomum denticulatum be eaten by a dog or wolf, the parasite passes into the nasal cavity of the
latter, and after further changes of cuticle becomes a fully-developed sexual Pentastomum taenioides, which does not differ to any very marked extent from P. denticulatum.
In their general characters the larval migrations of Pentastomum are similar to those of the Cestodes.
The internal anatomy of the adult Pentastomum, as well as the characters of the larva with two pairs of clawed appendages, are perhaps sufficient to warrant us in placing it with the Arthropoda, though it would be difficult to shew that it ought not to be placed with such a form as Myzostomum (vide p. 369). There do not appear to be any sufficient grounds to justify its being placed with the Mites amongst the Arachnida. If indeed the rings of the body of the Pentastomida are to be taken as implying a true segmentation, it is clear that the Pentastomida cannot be associated with the Mites.
(539) P. J. van Beneden. " Recherches s. 1'organisation et le developpement d. Linguatules." Ann. d. Sden. Nat., 3 Ser., Vol. XI.
(540) R. Leuckart. " Bau u. Entwicklungsgeschichte d. Pentastomen." Leipzig and Heidelberg. 1860.
Very little is known with reference to the development of the Tardigrada. A complete and regular segmentation (von Siebold, Kaufmann, No. 541) is followed by the appearance of a groove on the ventral side indicating a ventral flexure. At about the time of the appearance of the groove the cells become divided into an epiblastic investing layer and a central hypoblastic mass.
The armature of the pharynx is formed very early at the anterior extremity, and the limbs arise in succession from before backwards.
The above imperfect details throw no light on the systematic position of this group.
(541) J. Kaufmann. " Ueber die Entwicklung u. systematische Stellung d. Tardigraden." Zeit.f. wiss, ZooL, Bd. HI. 1851.
Summary of Arthropodan Development. The numerous characters common to the whole of the Arthropoda led naturalists to unite them in a common phylum, but the later researches on the genealogy of the Tracheata and Crustacea tend to throw doubts on this conclusion, while there is not as yet sufficient evidence to assign with certainty a definite position in either of these classes to the smaller groups described in the present chapter. There seems to be but little
doubt that the Tracheata are descended from a terrestrial Annelidan type related to Peripatus. The affinities of Peripatus to the Tracheata are, as pointed out in a previous chapter (p. 386), very clear, while at the same time it is not possible to regard Peripatus simply as a degraded Tracheate, owing to the fact that it is provided with such distinctly Annelidan organs as nephridia, and that its geographical distribution shews it to be a very ancient form.
The Crustacea on the other hand are clearly descended from a Phyllopod-like ancestor, which can be in no way related to Peripatus.
The somewhat unexpected conclusion that the Arthropoda have a double phylum is on the whole borne out by the anatomy of the two groups. Without attempting to prove this in detail, it may be pointed out that the Crustacean appendages are typically biramous, while those of the Tracheata are never at any stage of development biramous 1 ; and the similarity between the appendages of some of the higher Crustacea and those of many Tracheata is an adaptive one, and could in no case be used as an argument for the affinity of the two groups.
The similarity of many organs is to be explained by both groups being descendants of Annelidan ancestors. The similarity of the compound eye in the two groups cannot however be explained in this way, and is one of the greatest difficulties of the above view. It is moreover remarkable that the eye of Peripatus 2 is formed on a different type to either the single or compound eyes of most Arthropoda.
The conclusion that the Crustacea and Tracheata belong to two distinct phyla is confirmed by a consideration of their development. They have no doubt in common a centrolecithal segmentation, but, as already insisted on, the segmentation is no safe guide to the affinities.
In the Tracheata the archenteron is never, so far as we know, formed by an invagination 3 , while in Crustacea the
1 The biflagellate antennae of Pauropus amongst the Myriapocls can hardly be considered as constituting an exception to this rule.
3 I hope to shew this in a paper I am preparing on the anatomy of Peripatus.
8 Stecker's description of an invagination in the Chilognatha cannot be accepted without further confirmation ; -vide p. 388.
evidence is in favour of such an invagination being the usual, and, without doubt, the primitive, mode of origin.
The mesoblast in the Tracheata is formed in connection with a median thickening of the ventral plate. The unpaired plate of mesoblast so formed becomes divided into two bands, one on each side of the middle line.
In both Spiders and Myriopods, and probably Insects, the two plates of mesoblast are subsequently divided into somites, the lumen of which is continued into the limbs.
In Crustacea the mesoblast usually originates from the walls of the invagination, which gives rise to the mesenteron.
It does not become divided into two distinct bands, but forms a layer of scattered cells between the epiblast and hypoblast, and does not usually break up into somites ; and though somites are stated in some cases to be found they do not resemble those in the Tracheata.
The proctodaeum is usually formed in Crustacea before and rarely later 1 than the stomodaeum. The reverse is true for the Tracheata. In Crustacea the proctodseum and stomodaeum, especially the former, are very long, and usually give rise to the greater part of the alimentary tract, while the mesenteron is usually short.
In the Tracheata the mesenteron is always considerable, and the proctodaeum is always short. The derivation of the Malpighian bodies from the proctodaeum is common to most Tracheata. Such diverticula of the proctodaeum are not found in Crustacea.
1 This is stated to be the case in Moina (Grobben).
ECHINODERMATA 1 .
THE development of the Echinodermata naturally falls into two sections:
(i) The development of the germinal layers and of the systems of organs; (2) the development of the larval appendages and the metamorphosis.
The Development of the Germinal Layers and of tJie Systems
The development of the systems of organs presents no very important variations within the limits of the group.
Holothuroidea. The Holothurians have been most fully studied (Selenka, No. 563), and may be conveniently taken as type.
The segmentation is nearly regular, though towards its close, and in some instances still earlier, a difference becomes apparent between the upper and the lower poles.
At the close of segmentation (fig. 247 A) the egg has a nearly spherical form, and is constituted of a single layer of columnar cells enclosing a small segmentation cavity. The lower pole is slightly thickened, and the egg rotates by means of fine cilia.
An invagination now makes its appearance at the lower pole (fig. 247 B), and simultaneously there become budded off from tJie cells undergoing the invagination amoeboid cells, which
1 The following classification of the Echinodermata is employed in this chapter.
I. Holothuroidea. IV. Echinoidea.
II. Asteroidea. V. Crinoidea.
eventually form the muscular system and the connective tissue. These cells very probably have a bilaterally symmetrical origin. This stage represents the gastrula stage which is common to all Echinoderms. The invaginated sack is the archenteron. As it grows larger one side of the embryo becomes flattened, and the other more convex. On the flattened side a fresh invagination
FIG. 247. TWO STAGES IN THE DEVELOPMENT OF HOLOTHURIA TUBULOSA
VIEWED IN OPTICAL SECTION. (After Selenka.) A. Blastosphere stage at the close of segmentation. B. Gastrula stage. mr. micropyle ; //. chorion; s.c. segmentation cavity; bl. blastoderm; ep. epiblast; hy. hypoblast; ms. amoeboid cells derived from hypoblast ; a.e. archenteron.
arises, the opening of which forms the permanent mouth, the opening of the first invagination remaining as the permanent anus (fig. 248 A).
These changes give us the means of attaching definite names to the various parts of the embryo. It deserves to be noted in the first place that the embryo has assumed a distinctly bilateral form. There is present a more or less concave surface extending from the mouth to near the anus, which will be spoken of as the ventral surface. The anus is situated at the posterior extremity. The convex surface opposite the ventral surface forms the dorsal surface, which terminates anteriorly in a rounded prse-oral prominence.
It will be noticed in fig. 248 A that in addition to the primitive anal invagination there is present a vesicle (?/.). This vesicle is directly formed by a constriction of the primitive B. II. 35
archenteron (fig. 249 Vpv.), and is called by Selenka the vasoperitoneal vesicle. It gives origin to the epithelioid lining of the body cavity and water-vascular system of the adult 1 . In the parts now developed we have the rudiments of all the adult organs. The mouth and anal involutions (after the separation of the vaso-peritoneal vesicle) meet and unite, a constriction indicating their point of junction (fig. 248 B). Eventually the former gives
FIG. 248. THREE STAGES IN THE DEVELOPMENT OF HOLOTHURIA TUBULOSA
VIEWED FROM THE SIDE IN OPTICAL SECTION. (After Selenka.) tn. mouth; oe. oesophagus; st. stomach; i. intestine; a. anus; I.e. longitudinal ciliated band; v.p. vaso-peritoneal vesicle; p.v. peritoneal vesicle; p.r. right peritoneal vesicle ; //. left peritoneal vesicle ; w.v. water- vascular vesicle ; p. dorsal pore of water- vascular system ; ms. muscle cells.
rise to the mouth and cesophagus, and the latter to the remainder of the alimentary canal 2 .
The vaso-peritoneal vesicle undergoes a series of remarkable changes. After its separation from the archenteron it takes up a position on the left side of this, elongates in an anteroposterior direction, and from about its middle sends a narrow diverticulum towards the dorsal surface of the body, where an
1 The origin of the vaso-peritoneal vesicle is not quite the same in all the species. In Holothuria tubulosa it is separated from the csecal end of the archenteron; the remainder of which then grows towards the oral invagination. In Cucumaria the archenteron forks (fig. 249) ; and one fork forms the vaso-peritoneal vesicle, and the other the major part of the mesenteron.
2 There appears to be some uncertainty as to how much of the larval cesophagus is derived from the stomodaeal invagination.
opening to the exterior becomes formed (fig. 248 B, /.). The diverticulum becomes the madreporic canal, and the opening the dorsal pore.
The vaso-peritoneal vesicle next divides into two, an anterior vesicle (fig. 248 B, w.v.), from which is derived the epithelium of the water-vascular system, and a posterior (fig. 248 B, /.?;.), which gives rise to the epithelioid lining of the body cavity. The anterior vesicle (fig. 248 C, w.v.) becomes fivelobed, takes a horseshoe-shaped form, and grows round the oesophagus (fig. 256, w.v.r). The five lobes form the rudiments of the water-vascular prolongations into the tentacles. The remaining parts of the water-vascular system are also developed as outgrowths of the original vesicle. Five of these, alternating with the original diverticula, form the five ambulacral canals, from which diverticula are produced into the ambulacral feet ; a sixth gives rise to the Polian vesicle. The remaining parts of the original vesicle form the water-vascular ring.
We must suppose that eventually the madreporic canal loses its connection with the exterior so as to hang loosely in the interior, though the steps of this process do not appear to have been made out.
The original hinder peritoneal vesicle grows rapidly, and divides into two (fig. 248 C, pi. and pr.}, which encircle the two sides of the alimentary canal, and meet above and below it. The outer wall of each of them attaches itself to the skin, and the inner one to the alimentary canal and watervascular system ; in both cases the walls remain separated from the adjacent parts by a layer of the amoeboid cells already spoken of. The cavity of the peritoneal vesicles becomes the permanent body cavity. Where the walls of
FIG. 249. LONGITUDINAL SECTION
THROUGH AN EMBRYO OF CUCUMARIA DOLIOLUM AT THE END OF THE FOURTH DAY.
Vpv. vaso-peritoneal vesicle; ME. mesenteron; Blp., Ptd. blastopore, proctodaeum.
the two vesicles meet on the dorsal side, a mesentery, suspending the alimentary canal and dividing the body cavity longitudinally, is often formed. In other parts the partition walls between the two sacks appear to be absorbed.
The amoeboid cells, which were derived from the invaginated cells, arrange themselves as a layer round all the organs (fig. 249). Some of them remain amoeboid, attach themselves to the skin, and form part of the cutis; and in these cells the calcareous spicula of the larva and adult are formed. Others form the musculature of the larval alimentary tract, while the remainder give rise to the musculature and connective tissue of the adult.
The development of the vascular system is not known, but the discovery of Kowalevsky, confirmed by Selenka, that from the walls of the watervascular system corpuscles are developed, identical with those in the bloodvessels, indicates that it probably develops in connection with the watervascular system. The observations of Hoffmann and Perrier on the communication of the two systems in the Echinoidea point to the same conclusion. Though nothing very definite is known with reference to the development of the nervous system, Metschnikoff suggests that it develops in connection with the thickened bands of epiblast which are formed by a metamorphosis of the ciliated bands of the embryo, and accompany the five radial tubes (vide p. 555). In any case its condition in the adult leaves no doubt of its being a derivative of the epiblast.
From the above description the following general conclusions may be drawn :
(1) The blastosphere stage is followed by a gastrula stage.
(2) The gastrula opening forms the permanent anus, and the mouth is formed by a fresh invagination.
(3) The mesoblast arises entirely from the invaginated cells, but in two ways :
(a) As scattered amoeboid cells, which give origin to the muscles and connective tissue (including the cutis) of the body wall and alimentary tract.
(&) As a portion separated off from the archenteron, which gives rise both to the epithelioid lining of the body cavity, and of the water-vascular system.
(4) The oesophagus is derived from an invagination of the epiblast, and the remainder of the alimentary canal from the archenteron.
(5) The embryonic systems of organs pass directly into those of the adult.
The development of Synapta diverges, as might be expected, to a very small extent from that of Holothuria.
Asteroidea. In Asterias the early stages of development conform to our type. There arise, however, two bilaterally symmetrical vaso-peritoneal diverticula from the archenteron. These diverticula give rise both to the lining of the body cavity and water-vascular system. With reference to the exact changes they undergo there is, however, some difference of opinion. Agassiz (543) maintains that both vesicles are concerned in the formation of the water-vascular system, while Metschnikoff (560) holds that the watervascular system is entirely derived from the anterior part of the larger left vesicle, while the right and remainder of the left vesicle form the body cavity. MetschnikofFs statements appear to be the most probable. The anterior part of the left vesicle, after separating from the posterior, grows into a five-lobed rosette (fig. 260, /), and a madreporic canal (h] with a dorsal pore opening to the exterior. The rosette appears not to grow round the oesophagus, as in the cases hitherto described. But the latter is stated to disappear, and a new oesophagus to be formed, which pierces the rosette, and places the old mouth in communication with the stomach. Except where the anus is absent in the adult, the larval anus probably persists.
Ophiuroidea. The early development of the Ophiuroidea is not so fully known as that of other types. Most species have a free-swimming larva, but some (Amphiura) are viviparous.
The early stages of the free-swimming larvae have not been described, but I have myself observed in the case of Ophiothrix fragilis that the segmentation is uniform, and is followed by the normal invagination. The opening of this no doubt remains as the larval anus, and there are probably two outgrowths from this to form the vaso-peritoneal vesicles. Each of these divides into two parts, an anterior lying close to the oesophagus, and a posterior close to the stomach. The anterior on the right side aborts ; that on the left side becomes the water-vascular vesicle, early opens to the exterior, and eventually grows round the oesophagus, which, as in Holothurians, becomes the oesophagus of the adult. The posterior vesicles give rise to the lining of the body cavity, but are stated by Metschnikoff to be at first solid, and only subsequently to acquire a cavity the permanent body cavity. The anus naturally disappears, since it is absent in the adult. In the viviparous type the first stages are imperfectly known, but it appears that the blastopore vanishes before the appearance of the mouth. The development of the ^vaso-peritoneal bodies takes place as in the free-swimming larvae.
Echinoidea. In the Echinoidea (Agassiz, No. 542, Selenka, No. 564) there is a regular segmentation and the normal invagination (fig. 250 A). The amoeboid mesoblast cells arise as two laterally placed masses, and give rise to the usual parts. The archenteron grows forward and bends towards
the ventral side (fig. 250 B). It becomes (fig. 250 C) divided into three chambers, of which the two hindermost (d and c) form the stomach and intestine ; while the anterior forms the oesophagus, and gives rise to the
FIG. 250. THREE SIDE VIEWS OF EARLY STAGES IN THE DEVELOPMENT OF
STRONGYLOCENTRUS. (From Agassiz.)
a, anus (blastopore) ; d. stomach ; o. oesophagus ; c . rectum ; w. vaso-peritoneal vesicle ; v. ciliated ridge ; r. calcareous rod.
vaso-peritoneal vesicles. These latter appear as a pair of outgrowths (fig. 251), but become constricted off as a single two-horned vesicle, which subsequently divides into two. The left of these is eventually divided, as in Asteroids, into a peritoneal and water-vascular sack, while the right forms the right peritoneal sack. An oral invagination on the flattened ventral side meets the mesenteron after its separation from the vaso-peritoneal vesicle. The larval anus persists, as also does the larval mouth, but owing to the manner in which the water-vascular rosette is established the larval oesophagus appears to be absorbed, and to be replaced by a fresh oesophagus.
Crinoidea. Antedon, the only Crinoid so far studied (Gotte, No. 549), presents some not inconsiderable variations from the usual Echinoderm type. The blastopore is placed on the somewhat flattened side of the oval blastosphere, and not, as is usual, at the hinder end.
The blastopore completely closes, and is not converted into the permanent anus. The archenteron gives rise to the epithelioid lining of both body cavity and water-vascular system. These parts do not, however, appear as a single or paired outgrowth from the archenteron, but as three distinct outgrowths which are not formed contemporaneously. Two of them are first
FIG. -251. DORSO-VENTRAL VIEW OF AN EARLY LARVA OF STRONGYLOCENTRUS. (From Agassiz.)
a. anus ; d. stomach ; o. oesophagus ; w. vaso-peritoneal vesicle; r. calcareous rod.
formed and become the future body cavity; but their lumens remain distinct. Jngmally appearing as lateral outgrowths, the right one assumes a dorsal position and sends a prolongation into the stalk (fig. 252 rp'\ and the left one assumes first a ventral, and then an oral position (fur 252 lp\
The third outgrowth of the archenteron gives rise to the water-vascular vesicle. It first grows round the region of the future oesophagus and so forms the water-vascular ring. The wall of the ring then grows towards the body wall so as to divide the oral (left) peritoneal vesicle into two distinct vesicles, an anterior and a posterior, shewn in fig. 253, lp' and lp. Before this division is completed, the water-vascular ring is produced in front into five pro
FIG. 252. LONGITUDINAL SECTION THROUGH AN ANTEDON LARVA. (From Carpenter: after Gotte.)
al. mesenteron ; -wv. water- vascular ring ; lp. left (oral) peritoneal vesicle; rp. right peritoneal vesicle ; rp'. continuation of right vesicle into the stalk ; st. stalk.
cessesthe future tentacles (fig. 252, wv) which project into the cavity of the oral vesicle (lp\ After the oral peritoneal space has become completely divided into two parts, the anterior dilates (fig. 253, //) greatly, and forms a large vestibule at the anterior end of the body. This vestibule (lp'} next acquires a communication with the mesenteron, shewn in fig. 253 at m. The anterior wall of this vestibule is finally broken through. By this rupture the mesenteron is placed in communication with the exterior by the opening at m, while at the same time the tentacles of the water-vascular ring (/) project freely to the exterior. Such is Gotte's account of the prge-oral body space, but, as he himself points out, it involves our believing that the lining of the diverticulum derived from the primitive alimentary vesicle becomes part of the external skin. This occurrence is so remarkable, that more evidence appears to me requisite before accepting it.
The formation of the anus occurs late. Its position appears to be the same as that of the blastopore, and is indicated by a papilla of the mesenteron attaching itself to the skin on the ventral side (fig. 253, an). It eventually becomes placed in an interradial space within the oral disc of the adult. The water-vascular ring has no direct communication with the exterior, but the place of the madreporic canal of other types appears to be taken in the larva by a single tube leading from the exterior into the body cavity, the external opening of which is placed on one of the oral plates (vide p. 571) in the next interradial space to the right of the anus, and a corresponding diverticulum of the water-vascular ring opening into the body cavity. The line of junction between the left and right peritoneal vesicles forms in the larva a ring-like mesentery dividing the oral from the aboral part of the body
cavity. In the adult 1 the oral section of the larval body cavity becomes the ventral part of the circumvisceral division of the body cavity, and the subtentacular canals of the arms and disc ; while the aboral section becomes the dorsal part of the circumvisceral division of the body cavity, the cceliac canals of the arms, and the cavity of the centro-dorsal piece. The primitive
FIG. 253. LONGITUDINAL SECTION THROUGH THE CALYX OF AN ADVANCED PENTRACRINOID ANTEDON LARVA WITH CLOSED VESTIBULE.
(From Carpenter ; after Gotte.)
ae. epithelium of oral vestibule; ;//. mouth; al. mesenteron; an. rudiment of permanent anus; lp. posterior part of left (oral) peritoneal sack; lp' '. anterior part of left (oral) peritoneal sack; wr. water-vascular ring; /. tentacle; mt. mesentery; rp. right peritoneal sack; rp '. continuation of right peritoneal sack into the stalk; r. roof of tentacular vestibule.
distinction between the sections of the larval body cavity becomes to a large extent obliterated, while the axial and intervisceral sections of the bodycavity of the adult are late developments.
The more important points in the development indicated in the preceding pages are as follows :
(i) The blastosphere is usually elongated in the direction of the axis of invagination, but in Comatula it is elongated transversely to this axis.
1 Vide P. H. Carpenter, "On the genus Actinometra." Linnean Trans., and Series, Zoology, Vol. n., Part I., 1879.
(2) The blastopore usually becomes the permanent anus, but it closes at the end of larval life (there being no anus in the adult) in Ophiuroids and some Asteroids, while in Comatula it closes very early, and a fresh anus is formed at the point where the blastopore was placed.
(3) The larval mouth always becomes the mouth of the adult.
(4) The archenteron always gives rise to outgrowths which form the peritoneal membrane and water-vascular systems. In Comatula there are three such outgrowths, two paired, which form the peritoneal vesicles, and one unpaired, which forms the water-vascular vesicle. In Asteroids and Ophiuroids there are two outgrowths. In Ophiuroids both of these are divided into a peritoneal and a water-vascular vesicle, but the right watervascular vesicle atrophies. In Asteroids only one water-vascular vesicle is formed, which is derived from the left peritoneal vesicle. In Echinoids and Holothuroids there is a single vaso-peritoneal vesicle.
(5) The water- vascular vesicle grows round the larval oesophagus in Holothuroids, Ophiuroids, and Comatula ; in these cases the larval oesophagus is carried on into the adult. In other forms the water-vascular vesicle forms a ring which does not enclose the cesophagus (Asteroids and Echinoids); in such cases a new oesophagus is formed, which perforates this ring.
Development of the larval appendages and metamorphosis.
Holothuroidea. The young larva of Synapta, to which J. Muller gave the name Auricularia (fig. 255), is in many respects the simplest form of Echinoderm larva. With a few exceptions the Auricularia type of larva is common to the Holothuria.
It is (fig. 254 A and fig. 255) bilaterally symmetrical, presenting a flattened ventral surface, and a convex dorsal one. The anus (an) is situated nearly at the hinder pole, and the mouth (m) about the middle of the ventral surface. In front of the mouth is a considerable process, the prae-oral lobe. Between the mouth and anus is a space, more or less concave according to the age of the embryo, interrupted by a ciliated
A similar ciliated ridge is A E
ridge a little in front of the anus, present on the ventral surface of the prae-oral lobe immediately in front of the mouth. The anal and oral ridges are connected by two lateral ciliated bands, the whole forming a continuous band, which, since the mouth lies in the centre of it (fig. 255), may be regarded as a ring completely surrounding the body behind the mouth, or more naturally as a longitudinal ring.
The bilateral Auricularia is developed from a slightly elongated gastrula with an uniform covering of cilia. The gastrula becomes flattened on the oral side. At the same time the cilia become specially developed on the oral and anal ridges, and then on the remainder of the ciliated ring, while they are
FIG. 254. A. THE LARVA OF A HOLOTHUROID. B. THE LARVA OF AN ASTEROID.
- //. mouth; st. stomach; a. anus; l.c>
primitive longitudinal ciliated band; pr.c. prae-oral ciliated band.
FIG. 155. DIAGRAMMATIC FIGURES REPRESENTING THE EVOLUTION OF AN AURICULARIA FROM THE SIMPLEST ECHINODERM LARVAL FORM. (Copied from MUller.)
The black line represents the ciliated ridge. The shaded part is the oral side of the ring, the clear part the aboral side.
/;;. mouth; an. anus.
simultaneously obliterated elsewhere ; and so a complete Auricularia is developed. The water-vascular ring in the fully-developed larva has already considerably advanced in the growth round the oesophagus (fig. 256 w.v.r).
Most Holothurian larvae, in their transformation from the bilateral Auricularia form to the radial form of the adult, pass through a stage in which the cilia form a number of transverse
rings, usually five in number, surrounding the body. The stages in this metamorphosis are shewn in figs. 256, 257, and 258.
The primitive ciliated band, at a certain stage of the metamorphosis, breaks up into a number of separate portions (fig. 256), the whole of which are placed on the ventral surface. Four of these (fig. 257 A and B) arrange themselves in the form of an angular ring round the mouth, which at this period projects considerably. The remaining portions of the primitive band change their direction from a longitudinal one to a transverse (fig. 257 B), and eventually grow into complete rings (fig. 2570). Of these there are five. The middle one (257 B) is the first to develop, and is formed from the dorsal parts of the primitive ring. The two hinder rings develop next, and last of all the two anterior ones, one of which appears to be in front of the mouth (fig. 257 C).
The later development of the mouth, and of the ciliated ridge surrounding it, is involved in some obscurity. It appears from Metschnikoff (No. 560) that an invagination of the oesophagus takes place, carrying with it the ciliated ridge around the mouth. This ridge becomes eventually converted into the covering for the five tentacular outgrowths of the water- vascular ring (fig. 258), and possibly also forms the nervous system.
The opening of the cesophageal invagination is at first behind the foremost ciliated ring, but eventually comes to lie in front of it, and assumes a nearly terminal though slightly ventral position (fig. 258). No account has been given of the process by which this takes place, but the mouth is stated by Metschnikoff (though
FIG. 256. FULL-GROWN LARVA OF SYNAPTA. (After Metschnikoff.)
m. mouth ; st. stomach ; a. anus ; p.v. left division of perivisceral cavity, which is still connected with the watervascular system ; w.v.r. water-vascular ring which has not yet completely encircled the oesophagus; I.e. longitudinal part of ciliated band ; pr.c. prae-oral part of ciliated band.
Miiller differs from him on this point) to remain open throughout. The further changes in the metamorphosis are not considerable. The ciliated bands disappear, and a calcareous ring of ten pieces, five ambulacral and five interambulacral, is formed round the oesophagus. A provisional calcareous skeleton is also developed.
All the embryonic systems of organs pass in this case directly into those of the adult.
The metamorphosis of most Holothuroidea is similar to that just described. In Cucumaria (Selenka) there is however no Auricularia stage, and the uniformly ciliated stage is succeeded by one with five transverse
FIG. 257. THREE STAGES IN THE DEVELOPMENT OF SYNAPTA. A and B are viewed from the ventral surface, and C from the side. (After Metschnikoff.)
m. mouth; oe. oesophagus; pv. walls of the perivisceral cavity; wv. longitudinal vessel of the water- vascular system; p. dorsal pore of water-vascular system; cr. ciliated ring formed round the mouth from parts of the primitive ciliated band.
bands of cilia, and a prae-oral and an anal ciliated cap. The mouth is at first situated ventrally behind the prse-oral cap of cilia, but the prae-oral cap becomes gradually absorbed, and the mouth assumes a terminal position.
In Psolinus (Kowalevsky) there is no embryonic ciliated stage, and the adult condition is attained without even a metamorphosis. There appear to
be five plates surrounding the mouth, which are developed before any other part of the skeleton, and are regarded by P. H. Carpenter (No. 548) as equivalent to the five oral plates of the Crinoidea. The larval condition with ciliated bands is often spoken of as the pupa stage, and during it the larvae of Holothurians proper use their embryonic tube feet to creep about.
Asteroidea. The commonest and most thoroughly investigated form of Asteroid larva is a free swimming form known as Bipinnaria.
This form in passing from the spherical to the bilateral condition passes through at first almost identical changes to the Auricularian larva. The cilia become at an early period confined to an oral and anal ridge.
The anal ridge gradually extends dorsalwards, and finally forms a complete longitudinal post-oral ring (fig. 259 A) ; the oral ridge also extends dorsalwards, and forms a closed prae-oral ring (fig. 259 A), the space within which is left unshaded in my figure.
The presence of two rings instead of one distinguishes the Bipinnaria from the Auricularia. The two larvae are shewn side by side in fig. 254, and it is obvious that the two bands of the Bipinnaria are (as pointed out by Gegenbaur) equivalent to the single band of the Auricularia divided into two. Ontologically, however, the two bands of Bipinnaria do not appear to arise from the division of a single band.
As the Bipinnaria grows older, a series of arms grows out along lines of the two ciliated bands (fig. 259 C), and, in many cases, three special arms are formed, not connected with the ciliated bands, and covered with warts. These latter arms are
FlG. 258. A LATE STAGE IN THE DEVELOPMENT OF SYNAPTA. (After Metschnikoff.)
The figure shews the vestibular cavity with retracted tentacles ; the ciliated bands ; the water-vascular system, etc.
p. dorsal pore of water-vascular system ; pv. walls of perivisceral cavity; ms. amoeboid cells.
known as brachiolar arms, and the larvae provided with them as Brachiolaria (fig. 259 D).
As a rule the following arms can be distinguished (fig. 259 C and D), on the hinder ring (Agassiz' nomenclature) a median anal pair, a dorsal anal pair, and a ventral anal pair, a dorsal oral pair, and an unpaired anterior dorsal arm ; on the prae-oral ring a ventral oral pair, and sometimes (Miiller) an unpaired anterior ventral arm.
The three brachiolar arms arise as processes from the base of the unpaired dorsal arm, and the two ventral oral arms. The extent of the development of the arms varies with the species.
FIG. 259. DIAGRAMMATIC REPRESENTATION OF VARIOUS FORMS OF ASTEROID LARWE. A, B, C, BIPINNARIA; D, BRACHIOLARIA. (Copied from Muller.) The black lines represent the ciliated bands ; and the shading the space between the prae-oral and the post-oral bands.
m. mouth; an. anus.
The changes by which the Bipinnaria or Brachiolaria becomes converted into the adult starfish are very much more complicated than those which take place in Holothurians. For an accurate knowledge of them we are largely indebted to Alex. Agassiz (No. 543). The development of the starfish takes place entirely at the posterior end of the larva close to the stomach.
On the right and dorsal side of the stomach, and externally to the rig/it peritoneal space, are formed five radially situated calcareous rods arranged in the form of a somewhat irregular pentagon. The surface on which they are deposited has a spiral form, and constitutes together with its calcareous rods, the
abactinal or dorsal surface of the future starfish. Close to its dorsal, i.e. embryonic dorsal, edge lies the dorsal pore of the water-vascular system (madreporic canal), and close to its ventral edge the anus. On the left and ventral side of the stomach is placed the water-vascular rosette, the development of which was described on p. 549. It is situated on the actinal or ventral surface of the future starfish, and is related to the left peritoneal vesicle.
Metschnikoff (No. 560) and Agassiz (No. 543) differ slightly as to the constitution of the water- vascular rosette. The former describes and figures it as a completely closed rosette, the latter states that ' it does not form a completely closed curve but is always open, forming a sort of twisted crescent-shaped arc.'
The water-vascular rosette is provided with five lobes, corresponding to which are folds in the larval skin, and each lobe corresponds to one of the calcareous plates developed on the abactinal disc. The plane of the actinal surface at first meets that of the abactinal at an acute or nearly right angle. The two surfaces are separated by the whole width of the stomach. The general appearance of the larva from the ventral surface after the development of the water-vascular rosette (i) and abactinal disc (A) is shewn in fig. 260.
As development proceeds the abactinal surface becomes a firm and definite disc, owing to the growth of the original calcareous spicules into more or less definite plates, and to the development of five fresh plates nearer the centre of the disc and interradial in position. Still later a central calcareous plate appears on the abactinal surface, which is thus formed of a central plate, surrounded by a ring of five interradial plates, and then again by a ring of five radial plates. The abactinal disc now also grows out into five short processes, separated by five shallow notches. These processes are the rudiments of the five arms, and each of them corresponds to one of the lobes of the water-vascular rosette. A calcareous deposit is formed round the opening of the water-vascular canal, which becomes the madreporic tubercle 1 . At about this stage the absorption of the larval appendages takes place. The whole anterior part of the
1 The exact position of the madreporic tubercle in relation to the abactinal plates does not seem to have been made out. It might have been anticipated that it would be placed in one of the primary interradial plates, but this does not seem to be the case. The position of the anus is also obscure.
larva with the great prae-oral lobe has hitherto remained unchanged, but now it contracts and undergoes absorption, and becomes completely withdrawn into the disc of the future starfish. The larval mouth is transported into the centre of the actinal disc. In the larvae observed by Agassiz and Metschnikoff nothing was cast off, but the whole absorbed.
According to M tiller and Koren and Danielssen this is not the case in the larva observed by them, but part of the larva is thrown off, and lives for some time independently.
After the absorption of the larval appendages the actinal and abactinal surfaces of the young starfish approach each other, owing to the flattening of the stomach ; at the same time they lose their spiral form, and become flat discs, which fit each other. Each of the lobes of the rosette of the watervascular system becomes one of the radial water-vascular canals. It first becomes five-lobed, each lobe forming a rudimentary tube foot, and on each ^ d ctinal disc of youn Aste ' side of the middle lobe two fresh ones
next spring out, and so on in succession. The terminal median lobe forms the tentacle at the end of the arm, and the eye is developed at its base. The growth of the water-vascular canals keeps pace with that of the arms, and the tube feet become supported at their base by an ingrowth of calcareous matter. The whole of the calcareous skeleton of the larva passes directly into that of the adult, and spines are very soon formed on the plates of the abactinal surface. The original radial plates, together with the spines which they have, are gradually pushed outwards with the growth of the arms by the continual addition of fresh rows of spines between the terminal plate and the plate next to it. It thus comes about that the original radial plates persist at the end of the arms, in connection with the unpaired
FIG. 260. BIPINNARIA LARVA OF AN ASTEROID. (From Gegenbaur ; after Miiller.)
b. mouth ; a. anus ; h. madreporic canal ; t. ambulacral rosette ; c . stomach ; d. g. e. etc. arms of Bipinnaria ; A.
tentacles which form the apex of the radial water-vascular tubes.
It has already been mentioned that according to Metschnikoff (No. 560) a new oesophagus is formed which perforates the water-vascular ring, and connects the original stomach with the original mouth. Agassiz (No. 543) maintains that the water-vascular ring grows round the primitive oesophagus. He says " During the shrinking of the larva the long oesophagus becomes " shortened and contracted, bringing the opening of the mouth of the larva " to the level of the opening of the oesophagus, which eventually becomes "the true mouth of the starfish." The primitive anus is believed by Metschnikoff to disappear, but by Agassiz to remain. This discrepancy very possibly depends upon these investigators having worked at different species.
There is no doubt that the whole of the larval organs, with the possible exception of the oesophagus, and anus (where absent in the adult), pass directly into the corresponding organs of the starfish and that the prae-oral part of the body and arms of the larva are absorbed and not cast off.
In addition to the Bipinnarian type of Asteroid larva a series of other forms has been described by Miiller (No. 561), Sars, Keren, and Danielssen (No. 554) and other investigators, which are however very imperfectly known. The best-known form is one first of all discovered by Sars in Echinaster Sarsii, and the more or less similar larvae subsequently investigated by Agassiz, Busch, Miiller, Wyville Thomson, etc. of another species of Echinaster and of Asteracanthion. These larvae on leaving the egg have an oval form, and are uniformly covered by cilia. Four processes (or in Agassiz' type one process) grow out from the body ; by these the larvae fix themselves. In the case of Echinaster the larvae are fixed in the ventral concavity of the disc of the mother, between the five arms, where a temporary brood-pouch is established. The main part of the body is converted directly into the disc of the young starfish, while the four processes come to spring from the ventral surface, and are attached to the water- vascular ring. Eventually they atrophy completely. Of the internal structure but little is known ; till the permanent mouth is formed, after the development of the young starfish is pretty well advanced, the stomach has no communication with the exterior.
A second abnormal type of development is presented by the embryo of Pteraster miliaris, as described by Koren and Danielssen 1 . The larvae to the number of eight to twenty develop in a peculiar pouch on the dorsal surface of the body. The early stages are not known, but in the later ones the whole body assumes a pentagonal appearance with a mouth at one edge
1 The following statements are taken from the abstract in Bronn's Thierreichs. B. II. 36
of the disc. At a later stage the anus is formed on the dorsal side of an arm opposite the mouth. The stomach is surrounded by a water-vascular ring, from which the madreporic canal passes to the dorsal surface, but does not open. At a later stage the embryonic mouth and anus vanish, to be replaced by a permanent mouth and anus in the normal positions.
A third, and in some respects very curious, form is a worm like larva of Miiller, which is without bands of cilia. The dorsal surface of the youngest larva is divided by transverse constrictions into five segments. On the under side of the first of these is a five-lobed disc, each lobe being provided with a pair of tube feet.
At a later period only three segments are visible on the dorsal surface, but the ventral surface has assumed a pentagonal aspect. The later stages are not known.
Ophiuroidea. The full-grown larva of the Ophiuroids is known as a Pluteus. It commences with the usual more or less spherical form ; from this it passes to a form closely resembling
FIG. 261. DIAGRAMMATIC FIGURES SHEWING THE EVOLUTION OK AN OPHIUROID PLUTEUS FROM A SIMPLE ECHINODERM LARVA. (Copied from Miiller.) The calcareous skeleton is not represented.
///. mouth; an. anus; d. anterior arms; d'. lateral arms; e'. posterior arms; tf. anterolateral arms.
that of Auricularia with a rounded dorsal surface, and a flattened ventral one. Soon however it becomes distinguished by the growth of a post-anal lobe and the absence of a prae-oral lobe (fig. 261 B). The post-anal lobe forms the somewhat rounded apex of the body. In front of the mouth, and between the mouth and anus, arise the anal and oral ciliated ridges, which soon become continued into a single longitudinal ciliated ring. At the same time the body becomes prolonged into a series of
processes along the ciliated band, which is continued to the extremity of each. The primitive ciliated ring never becomes broken up into two or more rings. A ciliated crown is usually developed at the extremity of the post-anal lobe. The arms are arranged in the form of a ring surrounding the mouth, and are all directed forwards.
The first arms to appear are two lateral ones, which usually remain the most conspicuous (fig. 261 B and C, cf\ Next arises a pair on the sides of the mouth, which may be called the mouth or anterior arms (C, d}. A pair ventral to and behind the lateral arms is then formed, constituting the posterior arms (D, e'\ and finally a pair between the lateral arms and the anterior, constituting the anterolateral arms (D,^).
The concave area between the arms forms the greater part of the ventral surface of the body. Even before the appearance of any of the arms, and before the formation of the mouth, two calcareous rods are formed, which meet behind at the apex of the post-anal lobe, and are continued as a central support into each of the arms as they are successively formed. These rods are shewn at their full development in fig. 262. The important points which distinguish a Pluteus larva from the Auricularia or Bipinnaria are the following :
(i) The presence of the postanal lobe at the hind end of the body. (2) The slight development of a prae-oral lobe. (3) The provisional calcareous skeleton in the larval arms.
Great variations are presented in the development of the arms and provisional skeleton. The presence of lateral arms is however a distinctive characteristic of the Ophiuroid Pluteus. The other arms may be quite absent, but the lateral arms never.
The formation of the permanent Ophiuroid takes place in much the same way as in the Asteroidea.
FIG. 262. OPHIUROID. after Miiller.)
PLUTEUS LARVA OF AN (From Gegenbaur ;
A. rudiment of young Ophiuroid ; (?. lateral arms; d. anterior arms; e . posterior arms.
There is formed (fig. 262) on the right and dorsal side of stomach the abactinal disc supported by calcareous plates, at first only five in number and radial in position 1 . The disc is at first not symmetrical, but becomes so at the time of the resorption of the larval arms. It grows out into five processes the five future rays. The original five radial plates remain as the terminal segments of the adult rays, and new plates are always added between the ultimate and penultimate plate (Mu'ller), though it is probable that in the later stages fresh plates are added in the disc.
The ventral surface of the permanent Ophiuroid is formed by the concave surface between the mouth and anus. Between this and the stomach is
FIG. 263. DIAGRAMMATIC FIGURES SHEWING THE EVOLUTION OF ECHINOID PLUTEI. (Copied from Miiller.) The calcareous skeleton is not represented. E. Pluteus of Spatangus.
m. mouth; an. anus; d. anterior arms; d' . point where lateral arms arise in the Ophiuroid Pluteus; e. anterointernal arms; e. posterior arms; g'. anterolateral arms; g. anteroexternal arms.
situated the water-vascular ring. It is at first not closed, but is horseshoeshaped, with five blind appendages (fig. 262). It eventually grows round the cesophagus, which, together with the larval mouth, is retained in the adult. The five blind appendages become themselves lobed in the same way as in Asterias, and grow out along the five arms of the disc and become the radial canals and tentacles. All these parts of the water-vascular system are of course covered by skin, and probably also surrounded by mesoblast cells, in which at a later period the calcareous plates which lie ventral to the radial canal are formed. The larval anus disappears. As long as the larval appendages are not absorbed the ventral and dorsal discs of the permanent Ophiuroid fit as little as in the case of the Brachiolaria, but at a certain period the appendages are absorbed. The calcareous rods of the larval arms
1 Whether interradial plates are developed as in Asterias is not clear. They seem to be found in Ophiopholis bellis, Agassiz, but have not been recognised in other forms (vide Carpenter, No. 548, p. 369).
break up, the arms and anal lobe become absorbed, and the dorsal and ventral discs, with the intervening stomach and other organs, are alone left. After this the discs fit together, and there is thus formed a complete young Ophiuroid.
The whole of the internal organs of the larva (except the anus), including the mouth, cesophagus, the body cavity, etc. are carried on directly into the adult.
The larval skeleton is, as above stated, absorbed.
The viviparous larva of Amphiura squamata does not differ very greatly from the larvae with very imperfect arms. It does not develop a distinct ciliated band, and the provisional skeleton is very imperfect. The absence of these parts, as well as of the anus, mentioned on p. 549, may probably be correlated with the viviparous habits of the larva. With reference to the passage of this larva into the adult there is practically nothing to add to what has just been stated. When the development of the adult is fairly advanced the part of the body with the provisional skeleton forms an elongated rod-like process attached to the developing disc. It becomes eventually absorbed.
Echinoidea. The Echinus larva (fig. 263} has a Pluteus form like that of the Ophiuroids, and in most points, such as the
FIG. 264. Two LARV/E OF STRONGYLOCENTRUS. (From Agassiz.) m. mouth; a. anus; o. cesophagus; d. stomach; c. intestine; '. and v. ciliated ridges; iv. water- vascular tube; r. calcareous rods.
presence of the anal lobe, the ciliated band, the provisional skeleton, etc., develops in the same manner. The chief difference between the two Pluteus forms concerns the development of the lateral arms. These, which form the most prominent arms in the Ophiuroid Pluteus, are entirely absent in the Echinoid
Pluteus, which accordingly has, as a rule, a much narrower form than the Ophiuroid Pluteus.
A pair of ciliated epaulettes on each side of and behind the ciliated ring is very characteristic of some Echinoid larvae. They are originally developed from the ciliated ring (fig. 266 A
FIG. 265. LATERAL AND VENTRAL VIEW OF A LARVA OF STRONGYLOCENTRUS.
(From Agassiz.) General references as in fig. 264.
b. dorsal opening of madreporic canal; e '. posterior arms ; e'". anterior arms; f lV . anterointernal arms.
and B, z>"). The presence of three processes from the anal lobe supported by calcareous rods is characteristic of the Spatangoid Pluteus (fig. 263 E).
The first two pairs of arms to develop, employing the same names as in Ophiuroids, are the anterior attached to the oral process (fig. 263 C, d] and the posterior pair (*?') A pair of anterolateral arms next becomes developed (j^). A fourth pair (not represented in Ophiuroids) appears on the inner side of the anterior pair forming an anterointernal pair (e}, and in the Spatangoid Pluteus a fifth pair may be added on the external side of the anterior pair forming an anteroexternal pair (g).
Each of the first-formed paired calcareous rods is composed of three processes, two of which extend into the anterior and posterior arms ; and the third and strongest passes into the anal lobe, and there meets its fellow (fig. 265). A transverse bar in front of the arms joins the rods of the two sides meeting them at the point where the three processes diverge. The process in the anterolateral arm (fig. 266 B) is at first independent of this system of rods, but eventually unites with it. Although our knowledge of
the Pluteus types in the different groups is not sufficient to generalise with great confidence, a few points seem to have been fairly determined 1 . The Plutei of Strongylocentrus (figs. 266 and 267) and Echinus have eight arms and four ciliated epaulettes. The only Cidaris-like form, the Pluteus of which is known, is Arbacia : it presents certain peculiarities. The anal lobe develops a pair of posterior (auricular) appendages, and the ciliated ring, besides growing out into the normal eight appendages, has a pair of short blunt anterior and posterior lobes. An extra pair of non-ciliated accessory mouth arms appears also to be developed. Ciliated epaulettes are not present. So far as is known the Clypeastroid larva is chiefly characterized by the round form of the anal lobe. The calcareous rods are latticed. In the Pluteus of Spatangoids there are (fig. 263) five pairs of arms around the mouth pointing forwards, and three arms developed from the anal lobe pointing backwards. One of these is unpaired, and starts from the apex of the anal lobe. All the arms have calcareous rods which, in the case of the posterior pair, the anterolateral pair, and the unpaired arm of the anal lobe, are latticed. Ciliated epaulettes are not developed.
Viviparous larvae of Echinoids have been described by Agassiz 2 .
The development of the permanent Echinus has been chiefly worked out by Agassiz and Metschnikoff.
In the Pluteus of Echinus lividus the first indication of the adult arises, when three pairs of arms are already developed, as an invagination of the skin on the left side, between the posterior and anterolateral arms, the bottom of which is placed close to the water-vascular vesicle (fig. 266 B, u/\ The base of this invagination becomes very thick, and forms the ventral disc of the future Echinus. The parts connecting this disc with the external skin become however thin, and, on the narrowing of the external aperture of invagination and the growth of the thickened disc, constitute a covering for the disc, called by Metschnikoff the amnion. The water- vascular vesicle adjoining this disc grows out into five processes, forming as many tube feet, which cause the surface of the involuted disc to be produced into the same number of processes. The external opening of the invagination of the disc never closes, and after the development of the tube feet begins to widen again, and the amnion to atrophy. Through the opening of the invagination the tube feet now project. The dorsal and right surface of the Pluteus, which extends so as to embrace the opening of the madreporic canal and the anus, forms the abactinal or dorsal surface of the future Echinus (fig. 267, a). This disc fits on to the actinal invaginated surface which arises on the left side of the Pluteus. On the right surface of the larva (dorsal of permanent Echinus) two pedicellariae appear, and at a later period spines are formed, which are at first arranged in a ring-like form round the edge of the primitively flat test. While these changes are taking place, and the two surfaces of the future Echinus are gradually moulding themselves so as to
1 Vide especially Muller, Agassiz, and Metschnikoff.
2 For viviparous Echini vide Agassiz, Proc. Amer. Acad. 1876.
form what is obviously a young Echinus, the arms of the Pluteus with their contained skeleton have been gradually undergoing atrophy. They become irregular in form, their contained skeleton breaks up into small pieces, and they are gradually absorbed.
The water-vascular ring is from the first complete, so that, as in Asterias, it is perforated through the centre by a new oesophagus. According
FIG. 266. SIDE AND DORSAL VIEW OF A LARVA OF STRONGYLOCENTRUS.
(From Agassiz.) General reference letters as in figs. 264 and 265. e" . anterolateral arms; v" '. ciliated epaulettes; ?&'. invagination to form the disc of Echinus.
to Agassiz the first five tentacles or tube feet grow into the radial canals, and form the odd terminal tentacles exactly as in Asterias 1 . Spatangus only differs in development from Echinus in the fact that the opening of the invagination to form the ventral disc becomes completely closed, and that the tube feet have eventually to force their way through the larval epidermis of the amnion, which is ruptured in the process and eventually thrown off.
Crinoidea. The larva of Antedon, while still within the egg-shell, assumes an oval form and uniform ciliation. Before it
1 Gotte (No. 549) supported by Muller's and Krohn's older, and in some points extremely erroneous observations, has enunciated the view that the radial canals in Echinoids and Holothuroids have a different nature from those in Asteroids and Ophiuroids.
becomes hatched the uniform layer of cilia is replaced by four transverse bands of cilia, and a tuft of cilia at the posterior extremity. In this condition it escapes from the egg-shell
FIG. 267. FULL-GROWN LARVA OF STRONGYLOCENTRUS. (From Agassiz.) The figure shews the largely-developed abactinal disc of the young Echinus enclosing the larval stomach. Reference letters as in previous figs.
(fig. 268 A), and becomes bilateral, owing to a flattening of the ventral surface. On the flattened surface appears a ciliated
depression corresponding in position with the now closed blastopore (vide p. 550). The third ciliated band bends forward to pass in front of this (fig. 269). Behind the last ciliated band there is present a small depression of unknown function, also
FIG. 768. THREB STAGES IN THE DEVELOPMENT OF ANTEDON (COMATULA.)
(From Lubbock; after Thomson.)
A. larva just hatched; B. larva with rudiment of the calcareous plates; C. Pentacrinoid larva.
situated on the ventral surface. The posterior extremity of the embryo elongates to form the rudiment of the future stem, and a fresh depression, marking the position of the future mouth, makes its appearance on the anterior and ventral part.
While the ciliated bands are still at their full development, the calcareous skeleton of the future calyx makes its appearance in the form of two rows, each of five plates, formed of a network of spicula (figs. 268 B and 269). The plates of the anterior ring are known as the orals, those of the posterior as the basals. The former surround the left, i.e. anterior peritoneal sack ; the latter the right, i.e. posterior peritoneal sack. The two rows of plates are at first not quite transverse, but form two oblique circles, the dorsal end being in advance of the ventral. The rows soon become transverse, while the originally somewhat ventral oral surface is carried into the centre of the area enclosed by the oral plates.
By the change in position of the original ventral surface relatively to the axis of the body, the bilateral symmetry of the larva passes into a radial symmetry. While the first skeletal elements of the calyx are being formed, the skeleton of the stem is also established. The terminal plate is first of all established, then the joints, eight at first, of the stem. The centro-dorsal plate is stated by Thomson to be formed as the uppermost joint of the stem 1 . The larva, after the completion of the above changes, is shewn in fig. 268 B, and somewhat more diagrammatically in fig. 269.
After the above elements of the skeleton have become established the ciliated bands undergo atrophy, and shortly after 1 Gotte (No. 549) on the other hand holds that the centro-dorsal plate is developed by the coalescence of a series of at first independent rods, which originate simultaneously with, and close to, the lower edges of the basals, and that it is therefore similar in its origin to the basals.
FIG. 269. LARVA OF ANTEDON WITH RUDIMENTS OF CALCAREOUS SKELETON. (From Carpenter; after Thomson.)
i. Terminal plate at the end of the stem ; 3. basals ; or. orals ; bl. position of blastopore.
wards the larva becomes attached by the terminal plate of its stem. It then passes into the Pentacrinoid stage! The larva in this stage is shewn in fig. 268 C and fig. 270. New joints are added at the upper end of the stem next the calyx, and a new element the radials makes its appearance as a ring of five small plates, placed in the space between the basals and orals, and in the intervals alternating with them (fig. 270, 4). The roof of the oral vestibule (vide fig. 253 and p. 551) has in the meantime become ruptured ; and the external opening of the mouth thus becomes established. Surrounding the mouth are five petal-like lobes, each of them supported by an oral plate (fig. 268 C). In the intervals between them five branched and highly contractile tentacles, which were previously enclosed within the vestibule, now sprout out : they mark the position of the future radial canals, and are outgrowths of the water-vascular ring. At the base of each of them a pair of additional tentacles is soon formed. Each primary tentacle corresponds to one of the radials. These latter are therefore, as their name implies, radial in position; while the basals and orals are interradial. In addition to the contractile radial tentacles ten non-contractile tentacles, also diverticula of the water- vascular ring, are soon formed, two for each interradius.
In the course of the further development the equatorial space between the FlG - 2 7<>. YOUNG PEN . TACRINOID LARVA OF AN
orals and the basals enlarges, and gives TEDON. (From Carpenter ; rise to a wide oral disc, the sides of which after w >' ville Thom s"-)
- , , . ... . i. terminal plate of stem;
are formed by the radials resting on the c d. centro-donal plate; 3 . basals; while in the centre of it are bftsals J 4- radials; or. orals. placed the five orals, each with its special lobe.
The anus, which is formed on the ventral side in the position
of the blastopore (p. 551), becomes surrounded by an anal plate, which is interradial in position, and lies on the surface of the oral disc between the orals and radials. On the oral plate in the next interradius is placed the opening of a single funnel leading into the body cavity, which Ludwig regards as equivalent to the opening of the madreporic canal (vide p. 55 1) 1 .
From the edge of the vestibule the arms grow out, carrying with them the tentacular prolongation of the water-vascular ring. Two additional rows of radials are soon added.
The stalked Pentacrinoid larva becomes converted, on the absorption of the stalk, into the adult Antedon. The stalk is functionally replaced by a number of short cirri springing from the centro-dorsal plate. The five basals coalesce into a single plate, known as the rosette, and the five orals disappear, though the lobes on which they were placed persist. In some stalked forms, e.g. Rhizocrinus Hyocrinus, the orals are permanently retained. The arms bifurcate at the end of the third radial, and the first radial becomes in Antedon rosacea (though not in all species of Antedon) concealed from the surface by the growth of the centro-dorsal plate. An immense number of funnels, leading into the body cavity, are formed in addition to the single one present in the young larva. These are regarded by Ludwig as equivalent to so many openings of the madreporic canal ; and there are developed, in correspondence with them, diverticula of the water-vascular ring.
Comparison of Echinoderm Larvce and General Conclusions.
In any comparison of the various types of Echinoderm larvae it is necessary to distinguish between the free-swimming forms, and the viviparous or fixed forms. A very superficial examination suffices to shew that the free-swimming forms agree very much more closely amongst themselves than the viviparous
1 I have made no attempt to discuss the homologies of the plates of the larval Echinodermata because the criteria for such a discussion are still in dispute. The suggestive memoirs of P. H. Carpenter (No. 548) on this subject may be consulted by the reader. Carpenter attempts to found his homologies on the relation of the plates to the primitive peritoneal vesicles, and I am inclined to believe that this method of dealing with these homologies is the right one. Ludwig (No. 559) by regarding the opening of the madreporic canal as a fixed point has arrived at very different results.
COMPARISON OF ECHINODERM LARV.-E.
forms. We are therefore justified in concluding that in the viviparous forms the development is abbreviated and modified.
All the free forms are nearly alike in their earliest stage after the formation of the archenteron. The surface between the anus and the future mouth becomes flattened, and (except in Antedon, Cucumaria, Psolinus, etc. which practically have an abbreviated development like that of the viviparous forms) a ridge of cilia becomes established in front of the mouth, and a second ridge between the mouth and the anus. This larval form, which is shewn in fig. 264 A, is the type from which the various forms of Echinoderm larvae start.
In all cases, except in Bipinnaria, the two ciliated ridges soon become united, and constitute a single longitudinal postoral ciliated ring.
The larvae in their further growth undergo various changes, and in the later stages they may be divided into two groups :
(1) The Pluteus larva of Echinoids and Ophiuroids.
(2) The Auricularia (Holothuroids) and Bipinnaria (Asteroids) type.
The first group is characterized by the growth of a number of arms more or less surrounding the mouth, and supported by calcareous rods. The ciliated band retains its primitive condition as a simple longitudinal band throughout larval life. There is a very small prae-oral lobe, while an anal lobe is very largely developed.
The Auricularia and Bi- A. B
pinnaria resemble each other in shape, in the development of a large prae-oral lobe, and in the absence of provisional calcareous rods ; but differ in the fact that the ciliated band is single in Auricularia (fig 271 A), and is double in Bipinnaria (fig. 271 B).
THUROID. B. THE LARVA OF AN ASTEa great tendency to develop RIAS.
soft arms; while in the Auri- . ' mouth; st. stomach; a. anus; I.e. , . ,_, , *_ 1-1- primitive longitudinal ciliated band; pr.c.
cularia the longitudinal ciliat- p r3 e-oral ciliated band.
THE LARVA OF A
ed band breaks up into a number of transverse ciliated bands. This condition is in .some instances reached directly, and such larvae undoubtedly approximate to the larvae of Antedon, in which the uniformly ciliated condition is succeeded by one with four transverse bands, of which one is prae-oral.
All or nearly all Echinoderm larvae are bilaterally symmetrical, and since all Echinodermata eventually attain a radial symmetry, a change necessarily takes place from the bilateral to the radial type.
In the case of the Holothurians and Antedon, and generally in the viviparous types, this change is more or less completely effected in the embryonic condition ; but in the Bipinnaria and Pluteus types a radial symmetry does not become apparent till after the absorption of the larval appendages. It is a remarkable fact, which seems to hold for the Asteroids, Ophiuroids, Echinoids, and Crinoids, that the dorsal side of the larva is not directly converted into the dorsal disc of the adult; but the dorsal and right side becomes the adult dorsal or abactinal surface, while the ventral and left becomes the actinal or ventral surface.
It is interesting to note with reference to the larvae of the Echinodermata that the various existing types of larvae must have been formed after the differentiation of the existing groups of the Echinodermata ; otherwise it would be necessary to adopt the impossible position that the different groups of Echinodermata were severally descended from the different types of larvae. The various special appendages, etc. of the different larvae have therefore a purely secondary significance; and their atrophy at the time of the passage of the larva into the adult, which is nothing else but a complicated metamorphosis, is easily explained.
Originally, no doubt, the transition from the larva to the adult was very simple, as it is at present in most Holothurians ; but as the larvae developed various provisional appendages, it became necessary that these should be absorbed in the passage to the adult state.
It would obviously be advantageous that their absorption should be as rapid as possible, since the larva in a state of transition to the adult would be in a very disadvantageous
576 COMPARISON OF ECHINODERM
position. The rapid metamorphosis, which we find in Asteroids, Ophiuroids, and Echinoids in the passage from the larval to the adult state, has no doubt arisen for this reason.
In spite of the varying provisional appendages possessed by Echinoderm larvae it is possible, as stated above (p. 574), to recognise a type of larva, of which all the existing Echinoderm larval forms are modifications. This type does not appear to me to be closely related to that of the larvae of any group described in the preceding pages. It has no doubt certain resemblances to the trochosphere larva of Chaetopoda, Mollusca, etc., but the differences between the two types are more striking than the resemblances. It firstly differs from the trochosphere larva in the character of the ciliation. Both larvae start from the uniformly ciliated condition, but while the prae-oral ring is almost invariable, and a peri-anal ring very common in the trochosphere; in the Echinoderm larva such rings are rarely found ; and even when present, i.e. the prae-oral ring of Bipinnaria and the terminal though hardly peri-anal patch of Antedon, do not resemble closely the more or less similar structures of the trochosphere. The two ciliated ridges (fig. 264 A) common to all the Echinoderm larvae, and subsequently continued into a longitudinal ring, have not yet been found in any trochosphere. The transverse ciliated rings of the Holothurian and Crinoid larvae are of no importance in the comparison between the trochosphere larvae and the larvae of Echinodermata, since such rings are frequently secondarily developed. Cf. Pneumodermon and Dentalium amongst Mollusca.
In the character of the prae-oral lobe the two types again differ. Though the prae-oral lobe is often found in Echinoderm larvae it is never the seat of an important (supra-oesophageal) ganglion and organs of special sense, as it invariably is in the trochosphere.
Nothing like the vaso-peritoneal vesicles of the Echinoderm larvae has been found in the trochosphere ; nor have the characteristic trochosphere excretory organs been found in the Echinoderm larvae.
The larva which most nearly approaches those of the Echinodermata is the larva of Balanoglossus described in the next chapter.
(542) Alex. Agassiz. Revision of the Echini. Cambridge, U.S. 1872 74.
(543) Alex. Agassiz. " North American Starfishes." Memoirs of the Museum of Comparative Anatomy and Zoology at Harvard College, Vol. v., No. i. 1877 (originally published in 1864).
(544) J. Barrois. " Embryogenie de 1'Asteriscus verruculatus " Journal dc VAnat. et Phys. 1879.
(545) A. Baur. Beitrdge zur Naturgeschichte d. Synapta digitata. Dresden, 1864.
(546) H. G. Bronn. Klassen u. Ordnungen etc. Strahlenthiere, Vol. II. 1860.
(547) W. B. Carpenter. "Researches on the structure, physiology and development of Antedon." Phil. Trans. CLVI. 1866, and Proceedings of the Roy. Soc., No. 166. 1876.
(548) P. H. Carpenter. " On the oral and apical systems of the Echinoderms." Quart. J. of Micr. Science, Vol. xvm. and xix. 18789.
(549) A. Gotte. " Vergleichende Entwicklungsgeschichte d. Comatula mediterranea." Arch, fur micr. Anat., Vol. xn. 1876.
(550) R. Greeff. "Ueber die Entwicklung des Asteracanthion rubens vom Ei bis zur Bipinnaria u. Brachiolaria." Schriften d. Gesellschaft zur Beforderung d. gesammten Natunvissenschaften zu Marburg, Bd. xn. 1876.
(551) R. Greeff. "Ueber den Bau u. die Entwicklung d. Echinodermen." Sitz. d. Gesell. z. Beforderung d. gesam. Naturwiss. zu Marburg, No. 4. 1879.
(552) T. H. Huxley. "Report upon the researches of Miiller into the anat. anddevel. of the Echinoderms." Ann. and Mag. of Nat. Hist., 2nd Ser., Vol. vin. 1851.
(553) Koren and Danielssen. "Observations sur la Bipinnaria asterigera. Ann. Scien. Nat., Ser. in., Vol. vii. 1847.
(554) Koren and Danielssen. "Observations on the development of the Starfishes." Ann. and Mag. of Nat. Hist., Vol. XX. 1857.
(555) A. Kowalevsky. " Entwicklungsgeschichte d. Holothurien. " Mhn.Ac. Petersbourg, Ser. VII., Tom. XL, No. 6.
(556) A. Krohn. "Beobacht. a. d. Entwick. d. Holothurien u. Seeigel." Miillers Archiv, 1851.
(557) A. Krohn. "Ueb. d. Entwick. d. Seesterne u. Holothurien." Miillcr's Archiv, 1853.
(558) A. Krohn. "Beobacht. lib. Echinodermenlarven." Mailer's Archiv, 1854.
(559) H. Ludwig. "Ueb. d. primar. Steinkanal d. Crinoideen, nebst vergl. anat. Bemerk. lib. d. Echinodermen." Zeit.f. wiss. ZooL, Vol. xxxiv. 1880.
(560) E. Metschnikoff. "Studien iib. d. Entwick. d. Echinodermen u. Nemertinen." Mem. Ac. Petersboiirg, Series vii., Tom. xiv., No. 8. 1869.
(561) 1 Joh. Miiller. "Ueb. d. Larven u. d. Metamorphosed. Echinodermen." Abhandlungen d. Berlin. Akad. (Five Memoirs), 1848, 49, 50, 52 (two Memoirs).
(562) Joh. Mtiller. "Allgemeiner Plan d. Entwicklung d. Echinodermen." Abhandl. d. Berlin. Akad., 1853.
1 The dates in this reference are the dates of publication. B. II. 37
(563) E. Selenka. "Zur Entwicklung d. Holothurien." Zeit. f. wiss. Zool., Bd. xxvii. 1876.
(564) E. Selenka. "Keimblatter u. Organanlage bei Echiniden." Zeit.f.-wiss. Zool., Vol. xxxin. 1879.
(565) Sir Wyville Thomson. "On the Embryology of the Echinodermata." Natural History Review, 1 864.
(566) Sir Wyville Thomson. "On the Embryogeny of Antedon rosaceus." Phil. Trans. 1865.
THE larva of Balanoglossus is known as Tornaria. The prselarval development is not known, and the youngest stage (fig. 272) so far described (Gotte, No. 569) has many remarkable points of resemblance to a young Bipinnaria.
A mouth (m\ situated on the ventral surface, leads into an alimentary canal with a terminal anus (an). A prae-oral lobe is well developed, as in Bipinnaria, but there is no post-anal lobe. The bands of cilia have the same general form as in Bipinnaria. There is a prae-oral band, and a longitudinal post-oral band ; and the two bands nearly meet at the apex of the praeoral lobe (fig. 273). A contractile band
FIG. 272. EARLY STAGE IN THE DEVELOPMENT OF TORNARIA. (After Gotte.)
W. so-called watervascular vesicle developing as an outgrowth of the mesenteron; m.
passes from the oesophagus to the apex of mouth; an. anus, the prae-oral lobe, and a diverticulum (fig. 272, W) from the alimentary tract, directed towards the dorsal surface, is present. Contractile cells are scattered in the space between the body wall and the gut.
In the following stage (fig. 274 A) a conspicuous transverse post-oral band of a single row of long cilia is formed, and the original bands become more sinuous. The alimentary diverticulum of the last stage becomes an independent vesicle opening by a pore on the dorsal surface (fig. 274 A, w). The contractile cord is now inserted on this vesicle. Where this cord joins the apex of the prae-oral lobe between the two anterior bands of cilia a thickening of the epiblast (? a ganglion) has become
FIG. 273. YOUNG TORNARIA.
m. mouth ; an. anus ; w. watervascular vesicle ; oc. eye-spots ; c.c. contractile cord.
established, and on it are placed two eye-spots (fig. 273 oc, and fig. 274 A). A deep bay is formed on the ventral surface of the larva.
As the larva grows older the original bands of cilia become more sinuous, and a second transverse band with small cilia is formed (in the Mediterranean larva) between the previous transverse band and the anus. The water-vascular vesicle is prolonged into two spurs, one on each side of the stomach. A pulsating vesicle or heart is also formed (fig. 274 B, ht), and arises, according to Spcngel (No. 572), as a thickening of the epidermis. It subsequently becomes enveloped in a pericardium, and is placed in a depression in the water-vascular vesicle. Two pairs of diverticula, one behind the other, grow out (Agassiz, No. 568) from the gastric region of the alimentary canal. The two parts of each pair form flattened compartments, which together give rise to a complete investment of the adjoining parts of the alimentary tract. The two parts of each coalesce, and thus form
FlG. 274. TWO STAGKS IN THK 1 >KY KI.< >I'M KN I
OF TORNARIA. (After Metschnikoff.)
The black lines represent the ciliated hands. m. mouth; an. anus; br. branchial cleft; ///.
heart ; c. Ixxly cavity between splanchnic and
somatic mesoblast layers; 7.-'. watcr-vascvilar vesicle:
v. circular blood-vessel.
a double-walled cylinder round the alimentary tract, but their cavities remain separated by a dorsal and ventral septum.
Eventually (Spengel) the cavity of the anterior cylinder forms the section of the body cavity in the collar of the adult, and that of the posterior (fig. 274 B, c) the remainder of the body cavity. The septa, separating the two halves of each, remain as dorsal and ventral mesenteries.
The conversion of Tornaria (fig. 274 A) into Balanoglossus (fig. 274 B) is effected in a few hours, and consists mainly in certain changes in configuration, and in the disappearance of the longitudinal ciliated band.
The body of the young Balanoglossus (fig. 274 B) is divided into three regions (i) the proboscidian region, (2) the collar, (3) the trunk proper. The proboscidian region is formed by the elongation of the prae-oral lobe into an oval body with the eyespots at its extremity, and provided with strong longitudinal muscles. The heart (hi) and water-vascular vesicle lie near its base, but the contractile cord connected with the latter is no longer present. The mouth is placed on the ventral side at the base of the prae-oral lobe, and immediately behind it is the collar. The remainder of the body is more or less conical, and is still girt with the larval transverse ciliated band, which lies in the middle of the gastric region in the Mediterranean species, but in the cesophageal region in the American one.
The whole of the body, including the proboscis, becomes richly ciliated.
One of the most important cha- S us WITH FOUR BRANCHIAL racters of the adult Balanoglossus CLEFTS * (After Alex. Agossiz.)
r . m. mouth ; an. anus ; br. bran consists in the presence of respira- chial cleft . hL heart ; IV. watertory structures comparable with the vascular vesicle, vertebrate gill slits. The earliest traces of these structures are distinctly formed while the larva is still in the Tornaria
FIG. 275. LATE STAGE IN THE DEVELOPMENT OF BALANOGLOS
582 I'N I'KUOl'NKUSTA.
condition, as one pair of pouches from the oesophagus in the Mediterranean species, and four pairs in the American one (fig. 275, br).
In the Mediterranean Tornaria the two pouches meet the skin dorsally, and in the young Balanoglossus (fig. 274 B, br) acquire an external opening on the dorsal side. In the American species the first four pouches are without external openings till additional pouches have been formed. Fresh gill pouches continue to be formed both in the American and probably the Mediterranean species, but the conversion of the simple pouches into the complicated gill structure of the adult has only been studied by Agassiz (No. 568) in the American species. It would seem in the first place that the structure of the adult gill slits is much less complicated in the American than in the Mediterranean species. The simple pouches of the young become fairly numerous. They are at first circular ; they then become elliptical, and the dorsal wall of each slit becomes folded ; subsequently fresh folds are formed which greatly increase the complexity of the gills. The external openings are not acquired till comparatively late.
Our knowledge of the development of the internal organs, mainly derived from Agassiz, is still imperfect. The vascular system appears early in the form of a dorsal and a ventral vessel, both pointed, and apparently ending blindly at their two extremities. The two spurs of the water-vascular vesicle, which in the Tornaria stage rested upon the stomach, now grow round the oesophagus, and form an anterior vascular ring, which Agassiz describes as becoming connected with the heart, though it still communicates with the exterior by the dorsal pore and seems to become connected with the remainder of the vascular system. According to Spengel (No. 572) the dorsal vessel becomes connected with the heart, which remains through life in the proboscis : the cavity of the water-vascular vesicle forms the cavity of the proboscis in the adult, and its pore remains as a dorsal (not, as usually stated, ventral) pore leading to the exterior.
The eye-spots disappear.
Tornaria is a very interesting larval form, since it is intermediate in structure between the larva of an Echinoderm and trochosphere type common to the Mollusca, Chxtopoda, etc. The shape of the body especially the form of the ventral depression, the character of the longitudinal ciliated band, the structure and derivation of the water-vascular vesicle, and the
formation of the walls of the body cavity as gastric diverticula, are all characters which point to a connection with Echinodcrm larvae.
On the other hand the eye-spots at the end of the prae-oral lobe 1 , the contractile band passing from the oesophagus to the eye-spots (fig. 273), the two posterior bands of cilia, and the terminal anus are all trochosphere characters.
The persistence of the prae-oral lobe as the proboscis is interesting, as tending to shew that Balanoglossus is the surviving representative of a primitive group.
(567) A. Agassiz. "Tornaria." Ann. Lyceum Nat. Hist.\u\. New York, 1866.
(568) A. Agassiz. "The History of Balanoglossus and Tornaria." Mem. Amer. Acad. of Arts and Stien., Vol. IX. 1873.
(569) A. Gotte. " Entwicklangsgeschichte d. Comatula Mediterranea." Archiv fur mikr. Anat., Bd. xii., 1876, p. 641.
(570) E. Metschnikoff. " Untersuchungen iib d. Metamorphose, etc. (Tornaria)." Zeit.fiir wiss. ZooL, Bd. xx. 1870.
(571) J. M tiller. " Ueb. d. Larven u. Metamor. d. Echinodermen." Berlin Akad., 1849 and 1850.
(572) J. W. Spengel. "Ban u. Entwicklung von Balanoglossus. Tagebl. d. Naturf. Vers. Miinchen, 1877.
1 It would be interesting to have further information about the fate of the thickening of epiblast in the vicinity of the eye-spots. The thickening should by rights be the supra-oesophageal ganglion, and it does not seem absolutely impossible that it may give rise to the dorso-median cord in the region of the collar, which constitutes, according to Spengel, the main ganglion of the adult.
Abdominalia, 459, 493, 499
Acanthosoma, 473, 474, 475
Acarina, 444, 454
Achtheres percarum, 490
Acineta, 7, 8
Acraspeda, 152, 165, 167, 178, 179, 182,
Actinia, 169, 171, 179 Actinophrys, 9
Actinotrocha, 315, 318, 363, 364 Actinozoa, 26, 102, 152, j66, 170, 171,
172, 176, 178, 179, 181, 182, 186 Actinula, 155 Aculeata, 421 ^Egineta flavescens, 158 yEginidae, 156, 158 ^Eginopsis Mediterranea, 158 /Equorea Mitrocoma, 182 Agalma, 163 Agelena, 436, 450 Agelena labyrinthica, 119, 438 Alciope, 74 Alcippidae, 499 Alcyonaria, 152 Alcyonidse, 167, 168 Alcyonidium mytili, 297, 300, 302 Alcyonium palmatum, 119, 148, 167, 182 Alima, 484, 486 Amoeba, 19, 20 Amphibia, 22, 54, 56, 59, 60, 63, 66, 74,
Amphioxus, 54, 56, 59, 61, 66, 93, 426 Amphipoda, 518 Amphiporus lactifloreus, 202 Amphistomum, 31
,, subclavatum, 205
Amphitrochae, 330 Amphiura squamata, 565
Anchorella, 108, 492, 520
Anelasma squalicola, 499
Annelida, 14, 25, 98, 503, 525
Anodon, 37, 38, 39, 100, 107, 259, 260,
265, 266, 268 Anopla, 189, 202 Anura, 5
Antedon, 568, 573, 574 Aphides, 15, 16, 76, 79, 116, 428, 429 Aphrodite, 42
Apis, 402, 407, 408, 412, 413 Aplysia, 99, 226, 238, 252, 253 Aplysinidaa, 146 Apoda, 459, 493 Aptera, 395, 420 Apus, 1 6, 79, 460, 463 Arachnida, 22, 114, 119, 413, 4.51, 435,
444, 454, 455, 458, 537, 539 Arachnitis, 171 Araneina, 50, 51, 436 Arbacia, 567 Area, 38 Archigetes, 218 Archizosea gigas, 494 Arenicola, 42
Argiope, 311, 312, 315, 317 Argonauta, 247, 248 Argulus, 492 Armata, 355 Arthropoda, 12, 16, 18, 22, 75, 77,79, 83,
108, no, 221, 382, 383, 434, 448,503,
5 2 5> 534 54', 54 2 Articulata, 311, 313, 316, 317 Ascaridiae, 371 Ascaris nigrovenosa, 16, 82
,, lumbricoides, 375 Ascetta, 144 Ascidia canina, 53 Ascidians, 74, 102, 208, 426 Asellus aquaticus, 112,120, 516 Astacus, 66, 465, 477, 511, 512, 513,
Asteracanthion, 69, 70, 561
Asterias, 20, 68, 69, 71, 78, 80, 84, 549,
564 Asteroidea, 35, 36, 544, 549, 557, 563,
576 Astnea, 169
Atax Bonzi, 445
Atlanta, 231, 240
Auricularia, 553, 554, 562, 574
Autolytus cornutus, 319, 343
Aves, 56, 59, 61, 64, 107. 109
Axolotl, 1 6
Balanoglossus, 576, 579, 581
Balanus balanoides, 75, 493
Belemnites, 252, 253
Bipinnaria, 557, 563, 574, 576, 579
Blatta, 374, 395
Bojanus, organ of, 264, 282
Bonellia, 20, 43, 44, 98, 324, 355, 358,
359 Bothriocephalus salmonis, 211
,, proboscideus, 212
Brachiella, 492 Brachiolaria, 558, 564 Brachiopoda, 311, 317, 318 Brachyura, 466, 480, 483 Branchiobdella, 42, 43, 346 Branchiogasteropoda, 272 Branchiopoda, 79, 459, 523, 524 Branchipus, 463, 524 Branchiura, 459, 492 Branchionus urceolaris, 221 Braula, 396 Uuccinum, 237, 280 Bulimus citrinus, 229 Bunodes, 169, 171 Buthus, 431
Calcispongiae, 138, 148
Calycophoridce, 152, 159
Calyptoblastic Hydroids, 184, 185
Calyptraea, 223, 280
Campanularidse, 183, 184
Capitclla, 330, 332
Carcinus Mcenas, 481, 483
Cardium, 260, 262
" pygmaeum, 262
Caryophyllium, 168, 171 pea, 165, 167
Cecidomyia, 15, 79, 416, 417, 429
Cephalopoda, 20, 40, 41, 102, 108, 109, 135. "5. 240, 242, 244, 250, 252, 253, 270, 271, 272, 274, 279, 282, 287
Cephalothrix galatheae, 202
Cercariae, 207, 208, 209
Cerianthus, 168, 171
Cestodes, 14, 29, 31, 32, 33, 189, 210, 212, 218, 313, 425, 541
Chaetopoda, 5, 18, 23, 41, 43, 44 , 54, 67, 209, 215, 270, 275, 307, 312, 317, 318, 319, 320, 326, 334, 33<S, 342, 346, 349, 350, 351, 364. 369. 33, 36, 408, 448, 457, 458, 521, 576,582
Chelifer, 434, 436, 442, 446, 454
Chermes, 15, 429
Chilognatha, 113, 387, 389, 391, 393,
Chilopoda, 387, 392, 394 Chilostomata, 292, 297, 298, 304, 305 Chironomus, 15, 378, 401, 402, 415, 416,
Chiton, 254, 256, 257, 273 Chordata, 5 Chrysaora, 165 Chthonius, 436 Cicada, 395
Cirripedia, 459, 492, 496,503, 509, 520 Cladocera, 459, 464, 519 Clausilia, 239 Clavella, 520 Clavularia crassa, 167 Cleodora, 241 Clepsine, 73, 346, 347, 349, 351, 352,
353, 354 Clio, 242, 278 Clubione, 436 Clupeidae, 64 Cobitis barbatula, 378 Coccida;, 429 Coccus, 50 Ccelebogyne, 79 Coelenterata, 3, 5, 13, 18, 26, 27, 2S, 35,
74, 93, 94, 126, 148, 170, 178,179, 1 80,
181, 191, 342
Ccenurus cerebralis, 213, 214 Coleochaete, 1 1
Coleoptera, 396, 402, 409, 412, 420, 421, ^5
Collembola, 395, 426 Comatula, 5, 552, 553 Condracanthus, ill, 120, 520 Conochilus volvox, 22 1 Convoluta, 32 Copepoda, 109, 120, 459, 460, 487, 489,
493, 496, 503, 509, 519 Corallium rubrum, 168, 182 Corethra, 422, 423, 424 Crangoninoe, 476 Crnniiuhv, 311 Craniata, 5, 6, 19, 20, 54, 56, 59, 6l, 62,
6 4 , 74, 102
Crinoidea, 35, 36, 544, 550, 568, 576 Criodilus, 321, 324, 328, 341
Crisia, 304 Crocodilia, 63
Crustacea, 5, 6, 18, 51, 66, 102, 109, 120, 458, 4 6 5> 487* 5<>2, 521, 524, 537, 541 Cryptophialus, 499, 509 Crystalloides, 163 Ctenophora, 26, 93, 102, 152, 173, 175,
177, 178, 179, 180, 181, 182 Ctenostomata, 292, 297, 298, 304, 305 Cucullarms elegans, 46, 75, 82, 371, 376 Cucumaria, 546, 556, 574 Cumaceae, 459, 465, 486, 506 Curculio, 421
Cyclas, 259, 260, 261, 265 Cyclops, 376, 377, 418, 489, 503 Cyclostomata, 102, -292, 304 Cymbulia, 241, 242
Cymothoa, 516, 517, 519, 520,524, 528 Cynipidae, 15, 421, 428 Cyphonautes, 297, 301, 304, 306, 308 Cypridina, 500, 502 Cysticercus cellulosce, 214, 217
,, fasciolaris, 216
,, limacis, 213
Daphnia, 79, 464
Dasychone, 331, 336
Decapoda, 66, 248, 459, 465, 469, 504,
Dendroccela, 32, 33, 189, 195, 196 Dentalium, 258, 576 Desmacidon, 147 Desor, type of, 196, 197, 201, 202, 204,
212, 424 Diastopora, 304 Dibranchiata, 225, 253 Dicyema, 9, 131, 134, 135, 136 Dimya, 225 Diphyes, 159 Diplozoon, 11, 209, 210 Diporpa, 210 Diptera, 49, 194, 204, 396, 401,402,407,
409, 412, 416, 420, 429 Discina radiata, 317 Discinidse, 311
Discophora, 18, 42, 165, 346, 383 Distomese, 189, 205, 425 Distomum, 31
,, cygnoides, 209
,, globiparum, 207
,, lanceolatum, 205 Dochmius duodenale, 375
,, trigonocephalus, 375 Donacia, 401 Dracunculus, 376, 377
Echinaster fallax, 23
,, Sarsii, 102, 561 Echinodermata, 5, 18, 24, 35, 74, 102,
325, 424, 544, 573, 574, 57 6 > 5 82 Echinoidea, 35, 36, 544, 549, 565, 576 Echinorhyncus, 379, 380
Echinus lividus, 83, 84, 88
Echiurus, 44 , 357, 358
Ectoprocta, 297, 306
Edriophthalmata, 459, 465
Elasmobranchii, 23, 56, 59, 61, 62, 64,
67, 105, 106. 107, 108, 109 Enopla, 189, 202 Entoconcha mirabilis, 237 Entomophaga, 421
Entoprocta, 292, 298, 300, 302, 304, 306 Epeira, 436
Ephemera, 395, 409, 420, 422 Ephyra, 186
Epibulia auranliaca, 159, 165 Erichthus, 484, 507 Errantia, 319, 336 Esperia, 147 Estheria, 463, 464 Euaxes, lol, 322, 324, 341, 346,349 Eucharis, 178
,, multicornis, 178
Eucopepoda, 459 Eucope polystyla, 23, 154
Eunice sanguinea, 319
Eupagurus prideauxii, 112, 113, 115, 511, 520
Euphausia, 465, 468, 504, 505, 518, 523
Eurylepta auriculata, 192
Euspongia, 146, 147
Filaria, 377 Filaridae, 371 Firoloidea, 240 Flagellata, 7, 8 Flustrella, 301, 303 Formica, 396 Fungia, 182, 186 Fusus, 275, 280, 284, 288
Gammarus, 122, 518
,, fluviatilis, 117 ,, locusta, no, 112 Ganoids, 54, 102 Gasteropoda, 39, 41, 98, 225, 226, 229,
230, 232, 233, 240, 258, 260, 261, 270,
272, 275, 279, 283, 324 Gasterosteus, 64, 210 Gastrotricha, 370 Gasterotrochce, 330, 333 Gecarcinus, 465 Geophilus, 392, 393 Gephyrea, 5, 18, 24, 44, 54, 67, 102,
318, 320, 325, 355, 357, 361, 364 Germogen, 134 Geryonia hastata, 156 Geryonidse, 156 Glochidia, 267, 268 Gnathobdellidas, 346, 349 Gordiacea, 94
Cimlioidca, 371, 374, 378
- nia, 168
Gorgonidce, 181 Gorgoninrc, 181 Gregarinidae, 8 Gryllotalpa, 401, 412, 413 Gunnnineiv, 147, 148 Gymnoblastic Hydroids, 184, 185 Gymnoloemata, 292
Gymnosomata, 225, 240, 241, 242, 270 Gyrodactylus, 210
Ilalisarca, 22, 66, 145
Helix, 67, 229
Hemiptera, 395, 402, 403, 409, 420, 421
Hessia, 108, 492
Heterakis vermicularis, .374
Heteropoda, 71, 72, 225, 226, 231, 278
Hexacoralla, 152, 179, 182
Hippopodius gleba, 27, 159
Hirudinea, 74, 84
Hirudo, 350, 351, 352, 353, 354
Holometabola, 420, 422
Holothuria, 19, 25, 35, 549, 558, 576
Holothuroidea, 35, 544, 553, 556
Hyaleacea, 273, 275
Hydra, 21, 22, 26, 28, 29, 34, 152, 154,
155. 179, 183 Hydractinia, 539 Hydrocoralla, 152, 181, 185 Hydroidea, 152 Hydromedusae, 152, 179, 182, 183, 184,
185, 186, 187 Hydrophilus, 374, 396, 400, 401, 402,
404, 408, 409 Hydrozoa, 14, 19, 26, 27, 67, 102, 152,
155. 165. 179, 1 80, 181, 182, 539 Ilymenoptera, 396, 401, 402, 412, 420,
Inarticulata, 311, 316
Infusoria, 7, 8
Insecta, 5, 15, 18, 19, 25, 46, 395, 396,
4^5, 455. 45 Intoshia gigas, 136 Isidimc, 181 Ixxlyctia, 147 Isopoda, 109, 515, 519, 521, 523, 527
Julus Moneletei, 387, 388, 389 Kochlorine, 499
Lacertilia, 64 Lacinularia, 221, 223
socialis, 75 Lamellibranchiata, 23, 25, 37, 39, 98,
225, 241, 257, 258, 259, 269, 270, 271,
273, 274, 288 Lepadkue, 498
Lepas fascicularis, 224, 493, 494, 495 Lepidoptera, 79, 396, 402, 407, 408, 412,
413, 415, 417, 420, 421, 423, 415, 426.
Leptodora, 16, 51 Leptoplana, 74, 189, 192, 193 Lernseopoda, 490, 492, 520 Leucifer, 507
Libellulidae, 402, 403, 409, 420 Limax, 229, 232, 239, 278, 280 Limnadia, 79, 524 Limulus, 534 Lina, 402
Lingulidae, 311, 316 Lithobius, 393 Lobatse, 178
Loligo, 242, 243, 244, 247, 253 Loricata, 507, 514 Lota, 105
Loxosoma, 292, 294, 296, 306, 307 Lucernaria, 185 Lumbricus, 341, 368
,, agricola, 321
,, rubellus, 324
trapczoides, 13, 321, 323 Lumbriconereis, 334 Lymnseus, 82, 98, 226, 227, 232, 238,
281 Lycosa, 436
Macrostomum, 32, 34
Malacostraca, 66, 459, 462, 465, 504,
505, 506, 511, 523 Mammalia, 56, 58, 59, 64, 66 Marsipobranchii, 59 Mastigopus, 473, 474 Medusoe, 27, 154, 157, i.^s, 16;, 164, 176,
178, 181, 182, 183, 184, 185, 186 Megalopa, 482, 483, 484 Melolontha, 402, 421 Membranipora, 297, 303 Mermithido;, 371 Mesotrochoe, 330 Metachoetoe, 335 Metazoa, Q, 10, 12,67, 86, 125, 135, 14^,
Millepora, 152, 181
Mitraria, 308, 337
Mollusca, 5, 18, 24, 66, 74, 84, 99, 225, 247, 248, 251, 256, 257, 262, 271, 285, 288, 307, 325, 333, 352, 576, 582
Monomya, -225 Monostomum capitellum, 205
,, mutabile, 205, 206
Monotrochse, 330 Montacuta, 260, 262 Musca, 396 Muscidae, 420, 423 Myobia, 444, 445 Myrianida, 343 Myriapoda, 22, iir, 113, 387, 394, 395,
4i.3 458 Mynothela, 155 Myrmeleon, 396
Mysis, 120, 469, 472, 486, 504, 509, 525 Mytilus, 260, 261 Myxinoids, 5 Myxispongise, 145 Myzostomea, 369
Nassa mutabilis, 101, 226, 227, 233, 262,
278, 279, 288, 3^4 Natantia, 487 Natica, 237, 283 Nauplius, 5, 16, 460, 461, 463, 465, 466,
469, 473, 490, 491, 493, 497 Nautilus pompilius, 253, 276 Nebaliadse, 459, 465, 486 Nematoda, 45, 46, 50, 66, 74, 75, 371,
373. 374> 376 Nematogens, 131 Nematoidea, 18, 84, 94, 371, 374 Nematus ventricosus, 13, 427 Nemertea, 94, 189, 196, 202, 204 Nemertines, 30, 31, 33, 93, 136, 195,
202, 328, 333, 424 Nephelis, 82, 346, 349, 350, 351, 352,
,, diversicolor, 319
,, Dumerilii, 343 Neritina, 229, 237 Neuroptera, 396, 401, 420, 421 Neuroterus ventricularis, 428 Notonecta, 395 Nototrochse, 330, 353 Nudibranchiata, 229, 241
Octocoralla, 152, 179
Odontophora, 225, 257, 271
Oedogonium, 1 1
Oligochseta, 42, 319, 321, 325, 330, 338,
346, 352 Olynthus, 144 Oniscus murarius, 107, 108, 109, 120,
516, 520, 528 Opercula, 31 Ophiothryx, 36, 549 Ophidia, 64
Ophiuroidea, 136, 544, 553, 562, 565,
Ophryotrochoe puerilis, 333 Opisthobranchiata, 225, 232, 237 Ornithodelphia, 109 Orthonectidae, 136
Orthoptera, 395, 414, 420, 421, 425, 426 Ostracoda, 459, 500, 510 Ostrea, 259, 260, 262 Oxyuridse, 46, 373, 374 Oxyurus ambigua, 374 ,, vermicularis, 375
PcEcilopoda, 534 Paguridse, 477 Pakemon, no Palaemonetes, 476 Pakemoninre, 476, 511, 512 Palinurus, 478, 480
Paludina, 66, 227, 229, 235, 270, 278, 280
,, costata, 229
,, vivipara, 226 Pandorina, n Parasita, 489 Pedalion, 221
Pedicellina, 98, 292, 296, 299, 307 Pelagia, 167, 185 Penseinse, 476 Penaeus, no, 113, 465, 469, 473, 474,
Pennatulidae, 181 Pentacrinus, 5 Pentastomida, 539, 540 Pentastomum denticulatum, 540, 54!
tsenoicles, 539, 540, 541 Percidae, 64 PerennichaetcE, 335 Peripatus, 5, 386, 411, 412, 413, 542 Petromyzon, 61, 63, 64, 74, 83 Phalangella, 304 Phalangidse, 436 Phallusia, 83
Phascolosoma, 44, 355, 356, 361 Pholcus, 436, 442 Phoronis, 315, 355, 363, 364 Phoxinus laevis, 378 Phryganea, 396, 401, 409 Phylactokemata, 292, 294, 297, 305, 306 Phyllobothrium, 218 Phyllodoce, 329 Phyllopoda, 16, 459, 461, 505 Phyllosoma, 479, 480 Phylloxera, 429 Physophoridoe, 152, 16-2, 164 Pilidium, type of, 196, 200, 201, 202, 704,
Pisces, 5 Piscicola, 20, 43 Pisidium, 259, 260, 262, 264 Planaria Neapolitana, 193 Planorbis, 273, 281, 325
Platyelminthes, 18, 20, 24, 221, 424 Platygaster, 396, 416, 417, 418, 419 Pleurohrachia, 176, 177, 238 Pneumodermon, 242, 576 Podostomata, 292 Poduridce, 401, 405 Polychaeta, 42, 319, 325, 338 Polydesmus complanatus, 387, 388 Polygordius, 319, 325, 326, 327, 328,
332, 357 386 Polynoe, 42, 331 Polyophthalmus, 328 Polyplacophora, 225, 254, 270, 271, 288 Polystomeas, 189, 205, 209 Polystomum, 209
,, integerrimum, 30, 31, 210
Polytrochne, 330, 333 Polyxenia leucostyla, 158 Polyxenus lagurus, 387 Polyzoa, 98, 303, 305, 306. 30 8 > 3 ! 5. 3^ Porcellana, 483 Porifera, 102, 138, 148 Porthesia, 115 Prorhyncus, 32, 34 Prosobranchiata, 225, 237, 281 Prostomum, 32, 34, 38, 196 Protozoa, 8, 9, lo, n, 86, 135, 149 Protozoaea, 471 Protula Dysteri, 342 Pseudoneuroptera, 426 Pseudoscorpionid;e, 434 Psolinus, 556, 574 Psychidae, 16 Pteraster miliaris, 561 Pteropoda, 98, 225, 226, 229, 230, 232,
240, 258, 270, 272, 279, 283 Pterotrachcea, 71, 229, 240 Pulex, 396
Pulmonata, 39, 225, 232, 238, 281, 282 I'urpura lapillus, 78 Pycnogonida, 538 Pyrosoma, 13, 53, 109
Rana temporaria, 210 Kaspailia, 147 Rcdia, 206, 207, 208, 209 Reniera, 147
Kcptilia, 56, 59, 60, 61, 62, 64, 109 Rhabditis dolichura, 82 Khabdoccela, 32, 33, iSy, ic/> Khnbdopleura, 294, 306 Rhi/occphala, 459, 493, 499, 500 Klii/.ocrinus, 5 klii/.ostoma, 167 Rhomlx>gens, 131, 134 Khynchoncllidaj, 311 Rhyncdbddlkbe, 346 Rotifera, 5, 12, 18, 75, 76, 77, 79, 83, 102, 221, 308, 325
Saccocirrus, 328, 329, 332, 340 Sacculina, 500
Sagartia, 169, 171
Sagitta, 33, 74, 94, 130, 366, 367, 368
Seaphopoda, 225, 257, 270, 271
Schistocephalus, 2 1 1
Schizopoda, 459, 465, 466
Scorpio, 120, 43 r, 44 6, 454, 455, 457
Scrobicularia, 38, 39
Scyphistoma, 179, 185, 186
Sedentaria, 319, 336
Sepia, 20, 40, 41, 242, 243, 244, 245,
247> 2 49> 253 Sergestidce, 473, 507 Serpula, 319. 325, 331 Sertularia, 152, 183, 184 Silicispongia.', 147 Simulia, 401, 415 Siphonophora, 13, 77, 152, 159, 163,
165, 179, 1 80, 182, 185 Sipunculida, 24 Sipunculus, 44 Sirex, 396 Sitaris, 42!
Spathegaster baccarum, 428 Spjo, 4 2 > 33 2 > 333 Spiroptera obtusa, 376 Spirorbis Pagenstecheri, 319
spirillum, 319, 336 Spirula, 252 Spirulirostra, 252 Spongelia, 147 Spongida, 138, 144, 148, 149 Spongilla, 147, 150 Sporocysts, 206, 207, 208, 209 Squilla, 66, 504, 507 Stephanomia pictum, 162, 165 Stomalopoda, 459, 465, 4X4 Stomodoeum, 413 Strongylidrc, 371, 375 Strongylocentrus, 567 Strongysoloma Guerinii, 3<S7, 388, 390 Stylasterictae, 152, r8r Styliolidic, 24! Stylochopsis ponticus, 193 Sycandra, 93, 138, 144, 145, 147, 150
,, raphanus, i^S, 174 Syllis, 343
vivipara, 319 Sympodium coralloidcs, 168
Taeniatoe, 178 Tardigrada, 541 Teoenaria, 436
'I'clcDsti'i, IS, 25, 5^), 59, C>4. 107, io<) I'r].)troch;i.-, 330 Tcndra, 300 'I '(.'nth reds, 396 Tcrcbdla concliilcga, 332, 333, 337
Terebella nebulosa, 332, 333 Terebratula, 311, 315 Terebratulina, 311, 315, 316
,, septentrionalis, 315, 316
Teredo, larva of, 262 Tergipes, 232, 238
,, Edwardsii, 238 ,, lacinulatus, 238 Tethya, 147 Tetrabranchiata, 225 Tetranychus telarius, 116 Tetrastemma varicolor, 203 Thalassema, 44, 355, 357 Thalassinidae, 477 Thallophytes, n Thecidium, 311, 312, 315, 316 Thecosomata, 225 Thoracica, 459, 493, 499, 500 Thysanozoon, 192, 193 Thysanura, 395, 408, 425, 458 Tichogonia, 39 Tipula, 396 Tipulidae, 420, 421 Toenia cosnurus, 214
,, echinococcus, 215, 217
solium, 217 Tornaria, 579, 581 Toxopneustes, 22, 24, 35, 85, 88, 89 Tracheata, 385, 426, 432, 44 8, 455, 457,
458, 538, 54i
Trachymedusae, 152, 156, 179, 185 Trematodes, 14, 16, 29, 30, 31, 32, 33,
46, 94, 189, 205, 208, 210, 212, 216
Trichina, 377, 378
Trichocepha'lus affinis, 374
Trochosphsera aequatorialis, 221
Tubularia, 34, 38, 152, 154, 158
Tubularidse, 29, 179, 183
Tunicata, 5, I 4 , 53
Turbellaria, 5, 30, 31, 33, 74, 98, 102,
136, 179, 189, 193, 333 Tyroglyphus, 445
Unio, 37, 38, 39, 100, 101, 259, 260,265, 266, 445
Vaginulus luzonicus, 229
Vermes, 5, 74, 102, 223, 324, 352
Verongia rosea, 146
Vertebrata, 14, 18, 19, 24, 59, 64, 83,
272, 349. 397' 4^6 Vesiculata, 184 Vitrina, 229 Vorticella, 8, 9, 10
Wilsia, 164 Xiphoteuthis, 252
Zoantharia, 152, 168, 169 Zooea, 465, 468, 471, 474, 482, 483, 484, 486, 504
(1) } Ed. van Beneden. "Recherches sur la composition et la signification de ,A T m ' cour ' d ' l Acad " r y- des Sci <<* de Belgique, Vol. xxxiv. 1870.
/ '%, R- Leuckart. Artikel "Zeugung," R. WagMsfs Handworterbtek d. Physio logte, Vol. iv. 1853.
(3 ^ Fr ' L/ydig- , " Die Dotterfurchung nach ihrem Vorkommen in d. Thierwelt u. n. ihrer Bedeutung." Oken. Isis, 1848.
(4) Ludwig. "Ueber d. Eibildung im Thierreiche." Arbeiten a. d. zool.-zoot Institiit. Wiirzburg, Vol. I. rSy^.
(5) AllenThomson. Article ' ' Ovum " in Todd's Cyclopedia of Anatomy and Physiology, Vol. v. 1859.
(6) W. Waldeyer. Eierstock u. EL Leipzig, 1870.
THE OVUM OF CCELENTERATA.
(7) Ed. van Beneden. "De la distinction originelle d. testicule et de 1'ovaire." Bull. Acad. roy. Belgique, f serie, Vol. xxxvu. 1874.
(8) R. and O. Hertwig. Der Organismus d. Medusen. Jena, 1878.
(9) N. Kleinenberg. Hydra. Leipzig, 1872.
THE OVUM OF PLATYELMINTHES.
(10) P. Hallez. Contributions a fHistoire naturelle des Turbellarih. Lille, 1879.
(11) S. MaxSchultze. Beitrdge z. Naturgeschichte d. Turbellarien. Greifswald, 1851.
(12) C. Th. von Siebold. ' ' Helminthologische Beitrage." Miiller's Archiv, 1836.
(13) C. Th. von Siebold. Lehrbuch d. vergleich. Anat.d. wirbellosen Thiere. Berlin, 1848.
(14) E. Zeller. " Weitere Beitrage z. Kenntniss d. Polystomen." Zeit. f. wiss. ZooL, Bd. xxvu. 1876.
[Vide also Ed. van Beneden (No. i).]
THE OVUM OF ECHINODERMATA.
(15) C. K. Hoffmann. " Zur Anatomic d. Echiniden u. Spatangen." Niederllindisch. Archiv f. Zoologie, Vol. I. 1871.
(16) C. K. Hoffmann. " Zur Anatomic d. Asteriden. Niederldndisch. Ardiiv /. Zoologie, Vol. n. 1873.
(17) H. Ludwig. "Beitrage zur Anat. d. Crinoiden." Zeil. f. wiss. Zool., Vol. xxvin. 1877.
(18) Job. Miiller. "Ueber d. Canal in d. Eiern d. Holothurien." Miiller's Archiv, 1854.
(19) C. Semper. Holothurien. Leipzig, 1868.
(20) E. Selenka. Befruchtung d. Eies v. Toxopneustes variegalits, 1878.
[Vide also Ludwig (No. 4), etc.]
1 A very complete and critical account of the literature is contained in this paper. B. II. a
THE OVUM OF MOLLUSC A. Lamellibranchiata.
(21) II. Lacaze-Duthiers. " Organes genitaux des Acephales Lamellibranches." Ann. Set. Nat., 4 mc serie, Vol. 1 1. 1854.
(22) W. F lemming. " Ueb. d. er. Entwick. am Ei d. Teichmuschel." Archiv f. mikr. Anat., Vol. x. 1874.
(23) W. Flamming. "Studien lib. d. Entwick. d. Najaden." Sitz. d. t: Akad. Wiss. men, Vol. LXXI. 1875.
(24) Th. von Hassling. " Einige Bemerkungen, etc." Zeit. f. wiss. ZooL, Bd. v. 1854.
(25) H. von Jhering. "Zur Kenntniss d. Eibildung bei d. Muscheln." Zeit. f. wiss. ZooL, Vol. xxix. 1877.
(26) Keber. De Introihi Spermatozoorum in ovula, etc. Konigsberg, 1853.
(27) Fr. Leydig. " Kleinere Mittheilung etc." Miiller's Archiv, 1854.
(28) C. Semper. "Beitrage z. Anat. u. Physiol. d. Pulmonaten." Zeit. f. wiss. ZooL, Vol. vni. 1857.
(29) H. Eisig. " Beitrage z. Anat. u. Entwick. d. Pulmonaten." Zeit.f. wiss. ZooL, Vol. xix. 1869.
(30) Fr. Leydig. " Ueb. Paludina vivipara." Zeit.f. wiss. ZooL, Vol. u. 1850.
(31) Al. Kolliker. Entwicklungsgeschichte d. Cephalopoden. Zurich, 1844.
(32) E. R. Lankester. "On the Developmental History of the Mollusca." Phil. Trans., 1875.
THE OVUM OF THE CHJETOPODA.
(33) Ed. Claparede. " Les Annelides Chaetopodes d. Golfe de Naples." Mem.d. 1. Soctit. phys. eld 1 hist. nat. de Geneve, 1868 9 and 1870.
(34) E. Ehlers. Die Borstcnwiirmer nach system, und anat. Untersuchungen. Leipzig, 186468.
(35) E. Selenka. " Das Gefass-System d. Aphrodite aculeata." Niedcrldndisches Archiv f. ZooL, Vol. n. 1873.
THE OVUM OF DISCOPHORA.
(36) H. Dorner. " Ueber d. Gattung Branchiobdella." Zeit.f. wiss. ZooL, Vol. xv. 1865.
(37) R. Leuckart. Die menschlichen Parasiten.
(38) Fr. Leydig. "Zur Anatomie v. Piscicola eeometrica, etc." Zeit. f. wiss. ZooL, Vol. I. 1849.
(30) C. O. Whitman. "Embryology of Clepsine." Quart. 7. of Alter. Sci., Vol. xvin. 1878.
THE OVUM OF GEPHYREA.
(40) Keferstein u. Ehlers. Zoologische Beitrage. Leipzig, 1861.
(41) C. Semper. Holothurien, 1868, p. 145.
(42) J. W. Spengel. " Beitrage z. Kenntniss d Gephyreen." Beitriigc a. d. zool. Stationz. Neapcl, Vol. I. 1879.
(43) J. W. Spengel. " Anatomische Mittheilungen lib. Gephyreen." Tagcbl. d. Naturf. Vers. Munchen, 1877.
THE OVUM OF NEMATODA.
(44) Ed. Claparede. De la formation ct de la fccondaiiou dcs- n-uf.\ chcz Ics I'crs Ntmatodcs. (ienevc, 1859.
(J- r )) K. I. (.-nek art. Hif nirnsf/i lichen Paras! ten.
^' Nels0n * " On the reproduction of Ascaris mystax, etc." Phil. (48) A.Schneider. Monographie d.' Nematoden. Berlin, 1866. THE OVUM OF INSECT A.
Sm ' T? r u n d V Ueb ,?'* a5 Ei u ' seine Bildungsstdtte. Leipzig, 1 878. (50) T. H. Huxley. " On the agamic reproduction and morphology of Aphis. Ltnnean Trans., Vol. xxn. 1858. Vide also Manual of Invertebrate* Animals, 1877.
1 * ^ ^ ^ *
(51) bei den *,++,*
/-a\ ? r ',k ey< MS' Der Eierstock u. die Samentasche d. Insecten. Dresden, 1866. tSl ~ ub . bock - " The ov a and pseudova of Insects." Phil. Trans. 1850. (o4) Stem. Die weiblichen Geschlcchtsorgane d. Ktifer. Berlin, 1847. [Conf. also Glaus, Landois, Weismann, Ludwig (No. 4).]
THE OVUM OF ARANEINA.
(55) Victor Cams. " Ueb. d. Entwick. d. Spinneneies." Zeit. f. wiss. Zool. t Vol. ii. 1850.
(56) v. Wittich. "Die Entstehung d. Arachnideneies im Eierstock, etc." Miiller s Archiv, 1849.
[Conf. Leydig, Balbiani, Ludwig (No. 4), etc.]
THE OVUM OF CRUSTACEA.
(57) Aug. Weismann. "Ueb. d. Bildung von Wintereiern bei Leptodora hyalina." Zeit.f. wiss.ZooL, Vol. xxvn. 1876.
[For general literature vide Ludwig, No. 4, and Ed. van Beneden, No. i.]
THE OVUM OF CHORD ATA.
(58) A. Kowalevsky. " Weitere Studien ii. d. Entwicklung d. Ascidien." Archiv f. micr. Anat., Vol. VII. 1871.
(59) A. Kowalevsky. "Ueber Entwicklungsgeschichte d. Pyrosoma." Arch.f. micr. Anat., Vol. xi. 1875.
(60) Kupffer. " Stammverwandtschaft zwischen Ascidien u. Wirbelthieren." Arch. f. micr. Anat., Vol. VI. 1870.
(61) Giard. " Etudes critiques des travaux, etc. " Archives Zool. experiment., Vol. I. 1872.
(62) C. Semper. " Ueber die Entstehung, etc." Arbeiten a. d. zool.-zoot. Institut Wiirzburg, Bd. II. 1875.
(63) P. Langerhans. "Z. Anatomic d. Amphioxus lanceolatus," pp. 330 3. Archiv f. mikr. Anat., Vol. xil. 1876.
(64) F. M. Balfour. "On the structure and development of the Vertebrate Ovary." Quart. J. of Micr. Science, Vol. xvm. 1878.
(65) Th. Eimer. " Untersuchungen ii. d. Eier d. Reptilien." Arckiv f. mikr. Anat., Vol. vni. 1872.
(66) Pfliiger. Die Eierstbcke d. Sdugethiere u. d. Menschen. Leipzig, 1863.
(67) J. Foulis. " On the development of the ova and structure of the ovary in Man and other Mammalia." Quart. J. of Micr. Science, Vol. XVI. 1876.
(68) J. Foulis. " The development of the ova, etc." Journal of Anat. and Phys., Vol. xni. 18789.
(69) C. Gegenbaur. " Ueb. d. Bau u. d. Entwicklung d. Wirbelthiereier mit partieller Dottertheilung." Muller's Archiv, 1861.
(70) Alex. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.
(71) W. His. Untersuchungen iib. d. Ei u. d. Eientwicklung bei Knochenfischcn. Leipzig, 1873.
(72) A. Kolliker. Entwicklungsgeschichte d. Menschen u. hoherer Thicre, Leipzig, 1878.
(73) J. Miiller. " Ueber d. zahlreichen Porenkanale in d. Eikapsel d. Fische." Muller's Archiv, 1854.
(74) W. H. Ransom. " On the impregnation of the ovum in the Stickleback." Pro. K. Society, Vol. vn. 1854.
(75) C. Semper. " Das Urogenitalsystem d. Plagiostomen etc." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. II. 1875.
[Cf. Ludwig, No. 4, Ed. van Beneden, No. i, Waldeyer, No. 6, etc.]
MATURATION AND IMPREGNATION OF THE OVUM.
(76) Auerbach. Organologische Studien, Heft 2. Breslau, 1874.
(77) Bambeke. " Recherches s. Embryologie des Batraciens." Bull, de royale de Belgique, 2me ser., T. LXI. 1876.
(78) E. van Beneden. " La Maturation de 1'CEufdes Mammiferes." Bull, de fAcad. royale de Belgique, 2me ser., T. XL. No. 12, 1875.
(79) Id em. " Contributions a 1'Histoire de la Vesicule Germinative, &c." Bull, de fAcad. royale de Belgique, sme ser., T. XLI. No. i, 1876.
(80) O. Biitschli. Eizelle, Zelltheilung, und Conjugation der Infusorien. Frankfurt, 1876.
(81) F. M. Balfour. " On the Phenomena accompanying the Maturation and Impregnation of the Ovum." Quart. J. of Micros. Science, Vol. xvm. 1878.
(82) Calberla. " Befruchtungsvorgang beim Ei von Petromyzon Planeri.*' Zeit. f. iviss. Zool., Vol. xxx.
(83) W. Flemming. "Studien in d. Entwickelungsgeschichte der Najaden." Sitz. d. k. Akad. Wiett, B. LXXI. 1875.
(84) H. Fol. "Die erste Entwickelung des Geryonideneies. " Jenaische Zeitschrift, Vol. vn. 1873.
(85) Idem. " Sur le Developpement des Pte"ropodes." Archives de Zoologic Experimental et Gtnerale, Vol. iv. and v. 1875 6.
(86) Idem. " Sur le Commencement de 1'Henog^nie." Archives des Sciences Physiques et Naturelles. Geneve, 1877.
(87) Idem. Recherches s. I. Ftcondation etl. comrnen. d. rHcnogcnic. Geneve, 1879.
(88) R. Greeff. " Ueb. d. Bau u. d. Entwickelung d. Echinodermen." Sitzun. der Gesellschaft z. Befonlerung d. gesammten Naturwiss. z. Marburg, No. 5, 1876.
(89) Oscar Hertwig. " Beit. z. Kenntniss d. Bildung, &c., d. thier. Eies." Morphologisches Jahrbuch, Vol. I. 1876.
(90) Idem. Ibid. Morphologisches Jahrlntch, Vol. ill. Heft i, 1877.
(91) Idem. " Weitere Beitrage, &c." Morphologisches Jahrbuch, Vol. in. 1877. Heft 3.
(92) Idem. "Beit. z. Kenntniss, &c." Morphologisches Jahrbuch, Vol. iv. Heft i and 2. 1878.
(93) N. Kleinenberg. Hydra. Leipzig, 1872.
(94) C. Kupffer u. B. Benecke. Der Vorgang d. llcfnichtinig am Eie d. Neunaugen. Konigsberg, 1878.
(95) J. Oellacher. "Beitrage zur Geschichte des Keimblaschens im Wirbelthicreie." Archiv f. micr. Anat., Bd. VIII. 1872.
(%) W. Salensky. " Befruchtung u. P^urchung d. Sterlets-Eies." Zoologischer Anzeigcr, No. 11, 1878.
(97) E. Selenka. Befruchtung des Eies von Toxopncustcs variegatus. Leipzig, 1878.
fl Strasburger. Ucber Zclllnldu n- n. /.clltln ////;/;. Ji-na, 1876.
Idem. Utber Befrvehtung u. Zdlthdhing. Jena, 1X78.
(HiO) C. (). \V hi tin.in. "Tlic- Kniliryology of Clepsine." Quart. J. of A/i<r. Science, Vol. xvm. 1878.
DIVISION OF NUCLEUS.
(101) W. Flamming. "Beitrage z. Kenntniss d. Xclle u. ihrcr Lcbun.scrschcinungen." Archiv f. mikr. Anat., Vol. xvi. 1878.
(102) E. Klein. "Observations on the glandular epithelium and division of nuclei in the skin of the Newt." Quart, y. of Micr. Science, VoL XIX. 1879.
(103) Peremeschko. "Ueber d. Theilung d. thierischen Zellen." Archiv f. mikr. Anat., Vol. xvi. 1878.
(104) E. Strasburger. "Ueber ein z. Demonstration geeignetes ZclltheilungsObject." Sitz. d. Jenaischen Gesell.f. Med. u. Naturwiss., July 18, 1879.
(105) E. Haeckel. "Die Gastrula u. Eifurchung." Jenaische Ztitschrift, Vol. ix. 1877.
(106) Fr. Leydig. "Die Dotterfurchung nach ihrem Vorkommen in d. Thierwelt u. n. ihrer Bedeutung." Oken. /sis, 1848.
GENERAL WORKS ON EMBRYOLOGY.
(107) K. E. von Baer. " Ueb. Entwicklungsgeschichte d. Thiere." Konigsberg, 182837.
(108) C. Glaus. Grundziige d. Zoologie. Marburg und Leipzig, 1879.
(109) C. Gegenbaur. Grundriss d. vergleichenden Anatomie. Leipzig, 1878. Vide also Translation. Elements of Comparative Anatomy. Macmillan and Co., 1878.
(110) E. Haeckel. Studien z. Gastrcea-Theorie. Jena, 1877, and also Jenaische Zeitschrift, Vols. vni. and ix.
(111) E. Haeckel. Schopfungsgeschichte. Leipzig. Vide also Translation. The History of Creation. King and Co., London, 1876.
(112) E. Haeckel. Anthropogenie. Leipzig. Vide also Translation. Anthropogeny (Translation). Kegan Paul and Co., London, 1878.
(113) Th. H.Huxley. The Anatomy of Invertebrated Animals. Churchill, 1877.
(114) E. R. Lankester. "Notes on Embryology and Classification." Quart. J. of Micr. Science, Vol. xvi I. 1877.
(115) A. S. P. Packard. Life Histories of Animals, including Man, or Outlines of Comparative Embryology. Holt and Co., New York, 1876.
(116) H. Rathke. Abhandlungen z. Bildung- und Entwicklungsgesch. d. Menschen u. d. Thiere. Leipzig, 1833.
(117) E van Beneden. "Recherches sur les Dicyemides." Bull. d. FAcadtmie roy. de Belgique, f ser. T. XLI. No. 6 and T. XLII. No. 7, 1876. Vide this paper for a full account of the literature.
(118) A. K 611 ike r. Ueber Dicyema paradoxum den Schmarotzer der Venenanhiinge der Cephalopoden. ,
(119) Aug. Krohn. "Ueb. d. Vorkommen von Entozoen, etc. Fronep
Notizen, vn. 1839.
(120) A If. Giard. "Les Orthonectida classe nouv. d. Phylum des Vers." journal de tAnat. et de la Physiol., Vol. XV. 1879.
(121) El. Metschnikoff. "Zur Naturgeschichte d. OrthonecUdae." Zoologi scher Anzeiger, No. 40 43 l8 79 PORIFERA. '(122) C Barrois. " Embryologie de quelques eponges de la Manche. " An ""$) & &ZS^^'<t*>* SP"6es." A~* ^ M g . cf Nat. Hist., 4th series, Vol. xiv. 1874.
(124) Ganin 1 . " Zur Entwicklung d. Spongilla fluviatilis." Zoologischer Anzeigtr, Vol. i. No. 9, 1878.
(125) Robert Grant. "Observations and Experiments on the Structure and Functions of the Sponge." Edinburgh Phil. jf., Vol. xm. and XIV., 1825, 1816.
(126) E. Haeckel. Die Kalkschwamme, 1872.
(127) E. Haeckel. Studien zur Gastraa- Theorie. Jena, 1877.
(128) C. Keller. Unterstichungen iiber Anatomic und Entwicklungsgeschichte einiger Spongien. Basel, 1876.
(129) C. Keller. "Studien lib. Organisation u. Entwick. d. Chalineen." Zeit. f. wiss. Zoo/., Bd. xxvin. 1879.
(130) LieberkUhn. "Beitr. z. Entwick. d. Spongillen." Muller's Archiv, 1856.
(131) LieberkUhn. "Neue Beitrage zur Anatomie der Spongien." Miiller's Archiv, 1859.
(132) El. Metschnikoff. " Zur Entwicklungsgeschichte der Kalkschwamme. " Zeit.f. wiss. Zool., Bd. xxiv. 1874.
(133) El. Metschnikoff. "Beitrage zur Morphologic der Spongien." Zeit. f. wiss. Zool., Bd. xxvii. 1876.
(134) El. Metschnikoff. " Spongeologische Studien." Zeit. f. wiss. Zool., Bd. xxxn. 1879.
(135) Miklucho Maklay. "Beitrage zur Kenntniss der Spongien." Jenaische Zeitschrift, Bd. iv. 1868.
(136) O. Schmidt. "Zur Orientirung iiber die Entwicklung der Schwamme." Zeit.f. wiss. Zool., Bd. xxv. 1875.
(137) O. Schmidt. "Nochmals die Gastrula der Kalkschwamme." Archiv fur mikrosk. Anat., Bd. XII. 1876.
(138) O. Schmidt. "Das Larvenstadium von Ascetta primordialis und Asc. clathrus." Archiv fur mikrosk. Anatomie, Bd. xiv. 1877.
(139) F. E. Schulze. "Ueber den Bau und die Entwicklung von Sycandra raphanus." Zeit.f. wiss. Zool., Bd. xxv. 1875.
(140) F. E. Schulze. "Zur Entwicklungsgeschichte von Sycandra." Zeit. f. wiss. Zool., Bd. XXVII. 1876.
(141) F. E. S chulze. " Untersuchung Ub. d. Bau, etc. Die Gattung Halisarca." Zeit.f. wiss. Zoo/., Bd. xxvin. 1877.
(142) F. E. Schulze. "Untersuchungen iib. d. Bau, etc. Die Metamorphose von Sycandra raphanus." Zeit.f. wiss. Zool., Bd. xxxi. 1878.
(143) F. E. Schulze. "Untersuchungen u. d. Bau, etc. Die Familie Aplysinidae." Zeit.f. wiss. Zool., Bd. xxx. 1878.
(144) F. E. Schulze. "Untersuchungen u. d. Bau, etc. Die Gattung Spongelia." Zeit.f. wiss. Zool., Bd. xxxn. 1878.
(145) Alex. Agassi z. Illustrated Catalogue of the Museum of Comparative Anatomy at Harvard College, No. II. American Acalephac. Cambridge, U. S., 1865.
(140) O. and R. Hertwig. Der Organismus d. Medusa: u, seine Stellung z. Keimblattertheorie. Jena, 1878.
(147) A. Kowalevsky. "Untersuchungen lib. d. Entwicklung d. Coelenteraten." Nachrichten d. kaiser. Gcsell. d. Freunde d. Nattirerkenntniss d. Antliropologie u. Ethnographie. Moskau, 1873. (Russian). For abstract vide Jahresberichtc d. Anat. u. Phys. (Hoffman u. Schwalbe), 1873.
(148) L. A gas si z. Contributions to the Natural History of the United States of America. Boston, 1862. Vol. IV.
(149) G. J. Allman. A Monograph of the Gymnoblastic or Tubularian Hydrotds. Ray Society, 1871-2.
1 There is a Russian paper by the same author, containing a full account, with clear illustrations, of his observations.
(150) G. J. All man. "On the structure and development of Myriothela." Phil. Trans., Vol. CLXV. p. 2.
(Iff), P - J- van Beneden. "Mem. sur les Campanulaires de la Cote d'Ostende consideres sous le rapport physiologique, embryogenique, et zoologique." Nouv. Mini. de PAcad. de Brux., Tom. xvn. 1844.
(^ 2 ) p - J- van Beneden. "Recherches sur 1'Embryogenie des Tubulaires et 1 histoire naturelle des differents genres de cette famille qui habitent la Cote d'Ostende." Nouv. Mem. de P Acad. de Brux., Tom. xvii. 1844.
(153) C. Claus. "Polypen u. Quallen d. Adria." Denk. d. math.-naturwiss. Classe d. k. k. Akad. d. Wiss. Wien, Vol. xxxvin. 1877.
(154) J. G. Dal yell. Rare and Remarkable Animals of Scotland. London, 1847.
(* 55 ) , H - Fo1 - " Die er ste Entwicklung d. Geryonideneies." J 'enaische Zeit schrift, Vol. vn. 1873.
(156) Carl Gegenbaur. Zur Lehre vom Generationswechsel und der Fortpfianzung bei Medusen und Polypen. Wiirzburg, 1854.
(157) Thomas Hincks. "On the development of the Hydroid Polypes, Clavatella and Stauridia ; with remarks on the relation between the Polype and the Medusoid, and between the Polype and the Medusa." Brit. Assoc. Rep., 1861.
(158) E. Haeckel. Zur Entwicklungsgeschichte d. Siphonophoren. Utrecht, 1869.
(159) Th. H. Huxley. Oceanic Hydrozoa. Ray Society, 1858.
(160) Geo. Johnston. A History of British Zoophytes. Edin. 1838. 2nd Edition, 1847.
(161) N. Kleinenberg. Hydra, eine anatomisch-entwicklungsgeschichtliche Untersuchung. Leipzig, 1872.
(162) El. Metschnikoff. "Ueber die Entwicklung einiger Ccelenteraten." Bull, de FAcad. de St Petersbourg, XV. 1870.
(163) El. Metschnikoff. "Studien liber Entwicklungsgeschichte d. Medusen u. Siphonophoren." Zeit.f. wiss. ZooL, Bd. xxiv. 1874.
(164) H. N. Moseley. "On the structure of the Sty lasteridse." Phil. Trans.,
(165) F. E. Schulze. Ueber den Bau und die Entwicklung von Cordylophora lacustris. Leipzig, 1871.
(166) Al. Agassiz. "Arachnitis (Edwarsia) brachiolata." Proc. Boston Nat. Hist. Society, 1860.
(167) Koch. "Das Skelet d. Alcyonarien." Morpholog. Jahrbuch, Bd. iv. 1878.
(168) A. Kowalevsky. "Z. Entwicklung d. Alcyoniden, Sympodium coralloides und Clavularia crassa." Zoologischer Anzeiger, No. 38, 1879.
(169) H. Lacaze Duthiers. Histoire nat.du Cor ail. Paris, 1864.
(170) H. Lacaze Duthiers. " Developpement des Coralliaires." Archives de Zoologie experimental et generate, Vol. I. 1872 and Vol. u. 1873.
(171) C. Semper. " Ueber Generationswechsel bei Steinkorallen etc." Zeit. f. wiss. ZooL, Bd. xxii. 1872.
(172) Alex. Agassiz. "Embryology of the Ctenophorae." Mem. of the Anur. Acad. of Arts and Sciences, Vol. X. No. 1 1 1. 1874.
(173) G. J. All man. "Contributions to our knowledge of the structure and development of the Beroidse." Proc. Roy. Soc. Edinburgh, Vol. IV. 1862.
(174) C. Chun. "Das Nervensystem u. die Musculatur d. Rippenquallen." Abhand. d. Senkenberg. Gesellsch., B. XI. 1879.
(175) C. Claus. "Bemerkungen u. Ctenophoren u. Medusen." Zeit. f. wiss. ZooL, xiv. 1864.
(176) H. Fol. Ein Beitrag z. Anat. u. Entwickl. einiger Rippenquallen. 1869.
(177) C. Gegenbaur. "Studien u. Organis. u. System d. Ctenophoren." Archiv f. Naturgesch., xxii. 1856.
(178) A. Kowalevsky. " Entwicklungsgeschichte d. Rippenquallen. " Mtm. Acad. St Petersbourg, vii. serie, Tom. x. No. 4. 1866.
(179) J. Price. "Embryology of Ciliogrades." Proceed, of British Assoc., 1846.
(180) C. Semper. "Entwicklung d. Eucharis multicornis." Zeit. f. wtss. Zool., Vol. IX. 1858.
(181) Alex. Agassiz. "On the young stages of a few Annelids" (Planaria angitlata). Annals Lyceum Nat. Hist, of Neiv York, Vol. vin. 1866.
(182) Dalyell. "Powers of the Creator."
(183) C. Girard. "Embryonic development of Planocera elliptica." J our. of Acad. of Nat. Set., Philadelphia. New Series, Vol. II. 1854.
(184) Alex. Gotte. "Zur Entwicklungsgeschichte d. Seeplanarien." Zoologischer Anzeiger, No. 4, 1878.
(185) P. Halle z. Contributions a Thistoire naturelle des Turbellarits. Thesis a la facult^ des Sciences p. le grade d. Docteur es-sciences naturelles. Lille, 1879.
(186) Knappert. "Bijdragen tot de Ontwikkelings-Geschiedenis der Zoetwater-Planarien." Provinciaal Ulrechtsch Genootschap van Kunsten en Wetenschappen. Utrecht, 1865.
(187) W. Keferstein. " Beitrage z. Anat. u. Entwick. ein. Seeplanarien von St. Malo." Abh. d. konig. Gesell. d. Wiss. zu Gottingcn. Bd. XI v. 1868.
(188) El. Metschnikoff. " Untersuchungen lib. d. Entwicklung d. Planarien." Notizen d. neurussischen Gesellschaft d. Naturforscher. Odessa, Bd. V. 1877. Vide Hoffman and Schwalbe's Bericht for 1878.
(189) H. N. Moseley. "On Stylochus pelagicus and a new species of pelagic Planarian, with notes on other pelagic species, on the larval forms of Thysanozoon, etc." Quart. Journ. of Micr. Science, Vol. xvn. 1877.
(190) J. Miiller. "Ueber eine eigenthiimliche Wurmlarva a. d. Classe d. Turbellarien, etc." Miiller's Archiv f. Anat. u. Phys. 1850.
(191) J. Miiller. "Ueber verschiedene Formen von Seethieren." Miiller's Archiv f. Anat. und Phys. 1854.
(192) J. Barrois. " L'Embryologie des Nemertes." An. Sci. Nat., Vol. VI. 1877.
(193) O. BUtschli. Archiv f. Naturgeschichte, 1873.
(194) A. Krohn. "Ueb. Pilidium u. Actinotrocha." Miiller's Archiv, 1 858.
(195) E. Desor. "Embryology of Nemertes." Proceedings of the Boston Nat. History Society, Vol. VI. 1848.
(196) G. Dieck. "Entwicklungsgeschichte d. Nemertinen." Jenaische Zeitschrift, Vol. vin. 1874.
(197) C. Gegenbaur. "Bemerkungen lib. Pilidium gyrans, etc." Zeitschrift furwiss. Zool., Bd. v. 1854.
(198) C. K. Hoffman. "Entwicklungsgeschichte von Tetrastemma tricolor." Niederldndisches Archiv, Vol. ill. 1876, 1877.
(199) C. K. Hoffman. "Zur Anatomie und Ontogenie von Malacobdella." Niederldndisches Archiv, Vol. IV. 1877.
(200) W. C. M c Intosh. British Annelids. The Nemerteans. Ray Society, J873-4.
(201) Leuckart u. Pagenstecher. "Untersuchungen lib. niedere Seethiere." Miiller's Archiv, 1858.
(202) E. Metschnikoff. "Studien lib. die Entwicklung d. Echinodermen u. Nemertinen." Mhn. Acad. imp. Pttersbourg, vn. Ser., Tom. xiv. No. 8, 1869.
(203) T. S. Cobbold. Kntozoa. Groombridge and Son, 1864.
(204) T. S. Cobbold. Parasites; a Treatise on the Entozoa, etc. Churchill, 1879.
(205) F i 1 i p p i. " Mem. p. servir a 1'histoire geneHique des Tre"matodes." Ann. Scien. Nat., 4th Series, Vol. II. 1854, and Mem. Accad. Torino, 1855-1859.
206) R. Leuckart. Die menschlichen Parasilen, Vol. I. 1863, p. 485 ct seq.
207) H. A. Pagenstecher. Trematodtn u. Trematodenlarven. Heidelberg,
(208) C. Th. von Siebold. Lehrbuch d. vergleich. Anat. wirbelloser Thicre. Berlin, 1848.
( 209 ) J- J- S. Steenstrup. Generationswechsel. 1842.
(210) R. v. Willemoes-Suhm. "Zur Naturgeschichte d. Polystomuiu intcgerrimum, etc." Zeit.f. wiss. Zool., Vol. xxn. 1872.
(211) R. v. Willemoes-Suhm. Helminthologische Notizcn III." Zeit. f. wiss. Zool., Vol. xxiii. 1873. Vide this paper for a summary of known observations and literature.
(212) G. R. Wagener. Beitrdge zur Entwicklungsgeschichte d. Eingeweidewiirmer. Haarlem, 1855.
(213) G. R. W age n e r. " Helminthologische Bemerkungen, etc." Zeit. f. wiss. Zool., Vol. ix. 1850.
(214) G. R. Wagener. "Ueb. Gyrodactylus elegans." Archiv f. Anat. u. Phys. 1860.
(215) E. Zeller. " Untersuchungen ub. d. Entwicklung d. Diplozoon paradoxum." Zeit.f. wiss. Zool., Vol. xxn. 1872.
(216) E. Zeller. "Untersuchungen u. d. Entwick. u. Bau d. Polystomum integerrimum." Zeit.f. wiss. Zool., Vol. xxn. 1872.
(217) E. Zeller. "Weitere Beitrage z. Kenntniss d. Polystomen." Zeit.f. wiss. Zool., Vol. xxvn. 1876.
(218) Ed. van Beneden. "Recherches sur la composition et la signification d. 1'oeuf." Mem. cour. Acad. roy. Belgique. Vol. xxxiv. 1868.
(219) P. J. van Beneden. "Les vers Cestoi'des consideres sous le rapport physiologique embryogenique, etc." Bull. Acad. Scien. Bruxelles. Vol. xvn. 1850.
(220) T. S. Cobbold. Entozoa. Groombridge and Son, 1864.
(221) T. S. Cobbold. Parasites; a treatise on the Entozoa, etc. Churchill, 1879.
(222) Th. H. Huxley. "On the Anatomy and Development of Echinococcus veterinorum." Proc. Zool. Soc. Vol. xx. 1852.
(223) J. Knoch. "Die Naturgesch. d. breiten Bandwiirmer." Mem. Acad. Imp. Petersbourg, Vol. v. Ser. 7, 1863.
(224) F. Kiichenmeister. "Ueber d. Umwandlung d. Finnen Cysticerci in Bandwiirmer (Tsenien)." Prag. Vierteljahrsschr. 1852.
(225) F. Kiichenmeister. "Experimente iib. d. Entstehung d. Cestoden. 2 Stufe zunachst d. Ccenurus cerebralis." Giinsburg, Zeitsch. klin. Med. iv. 1853.
(226) R. Leuckart. Die menschlichen Parasiten, Vol. I. Leipzig, 1863. Vide also additions at the end of the ist and 2nd volume.
(227) R. Leuckart. "Archigetes Sieboldii, eine geschlechtsreife Cestodenamme." Zeit.f. wiss. Zool., Vol. xxx. Supplement, 1878.
(228) El. Metschnikoff. "Observations sur le developpement de quelques animaux (Bothriocephalus proboscideus). " Bull. Acad. Imp. St Petersbourg, Vol.
(229) 'w. Salensky. "Ueb. d. Bau u. d. Entwicklungsgeschichte d. Amphilina." Zeit.f. wiss. Zool., Vol. xxiv. 1874.
(230) Von Siebold. Burdach's Physiologie.
(231) R. von Willemoes-Suhm. "Helminthologische Notizen." Zfit. /. wiss. Zool., Vol. xix. xx. xxn. 1869, 70 and 73.
(232) F. Cohn. "Ueb. d. Fortpflanzung von Raderthiere." Zeit.f. wiss.
^(233) F. Cohn. "Bemerkungen u. Raderthiere." Zeit.f. wiss. Zool., Vol. IX. 1858, and Vol. xn. 1862.
(234) T. H. Huxley. "Lacinularia socialis." Trans, of the Microscopical
(235) Fr. Leyclig. " Ueb. d. Bau u. d. systematische Stelluny; d. Radcrthiere." Ztit.f. unss. Zool., Vol. vi. 1854.
(236) W. Salensky. "Beit. z. Entwick. von Brachionus urceolaris." Zeit. /. itnss. Zool., Vol. xxn. 1872.
(237) C. Semper. " Zoologische Aphorismen. Trochosphuera axjuatorialis." Zeit.f. wiss. Zool., Vol. xxn. 1872.
(238) T. H. Huxley. "On the Morphol. of the Cephal. Mollusca." Phil. Trans., 1853.
(239) E. R. Lankester. "On the developmental history of the Mollusca." Phil. Trans., 1875.
(240) H. G. Bronn and W. Keferstein. Die Klasscn u. Ordnungcn d. Thierreichs, Vol. III. 1862-1866.
Gasteropoda and Pteropoda.
(241) J. Alder and A. Hancock. "Devel. of Nudibr." Ann. and Magaz. Nat. Hist., Vol. XH. 1843.
(242) N. Bobretzky. "Studien iiber die embryonale Entwicklung d. Gasteropoden." Archivf. micr. Anat., Vol. xin.
(243) W. K. Brooks. "Preliminary Observations on the Development of Marine Gasteropods." Chesapeake Zoological Laboratory, Session of 1878. Baltimore, 1879.
(244) O. Biitschli. " Entwicklungsgeschichtliche Beitrage (Paludina vivipara)." Zeit.f. wiss. Zool., Vol. xxix. 1877.
(245) W. Carpenter. "On the devel. of the embr. of Purpura lapillus." Trans. Micros. Soc., 2 d series, Vol. ill. 1855.
(246) W. Carpenter. "On the devel. of the Purpura." Ann. and Mag. of Nat. Hist., 2 d series, Vol. xx. 1857.
(247) E. Claparede. "Anatomic u. Entwickl. der Neritina fluviatilis." MUller's Archiv, 1857.
(248) H. Eisig. "Beitr. z. Anat. u. Entwickl. der Geschlechtsorg. von Lymnieus." Zeitschr. f. wiss. Zool., Vol. xix. 1869.
(249) H. Fol. " Sur le developpement des Pteropodes." Archives de Zool. experim. et gtntrale, Vol. iv. 1875.
(250) H. Fol. " Sur le developpement des Gasteropodes pulmones." Compt. rend., 1875, pp. 523526.
(251) H. Fol. "Sur le developpement des Heteropodes." Archives de Zool. expe"rim.etgtn<b-ale,\o\.v. 1876.
(252) C. Gegenbaur. "Beit. z. Entwicklungsgesch. der Landgasteropoden." Zeitschr. f. w. Zool., Vol. ill. 1851.
(253) C. Gegenbaur. Untersuch. iib. Pteropoden u. Hetcropoden. Leipzig, '855.
(254) H. von Jhering. "Entwicklungsgeschichte von Helix." Jcnaische Zcitschrift, Vol. IX. 1875.
(255) W. Keferstein and E. Ehlers. "Beob. lib. d. Entwick. v. Molis peregr." Zool. Beitr., 1861.
(256) J. Koren and D. C. Danielssen. "Benuerk. til Mollusk. Udvikling." NytMag.f. Naturvidensk., Vol. v. 1847. -^"j P- 2O2> '848.
(257) J. Koren and D. C. Danielssen. liidrag til Pectinibr. Udvikl. licrgcn, 1851 (supplement, 1852). Ann. and Mag. Nat. Hist., 1857.
(258) A. Krohn. "Beobacht. aus d. Entwickl. der Pteropoden u. Heterop." Muller's Archiv, 1856 and 1857.
(259) A. Krohn. Beitr. zur Entwickl. der Pteropoden u. Heteropoden. Leipzig, 1860.
(260) H. de Lacaze-Duthiers. "Mem. sur 1'anat.et 1'embryog. des Vermets." 2 partie. Ann. sc. not., 4" srie, T. xm. 1860.
(261) P. Langerhans. "Zur Entwickl. der Gasterop. Opisthobr." Zeitschr. f. w. Zool., Vol. xxni. 1873.
. E. R. Lankester. "On the development of the Pond-Snail." Quart.
J. of Micr. Scie., Vol. xiv. 1874.
(263) E. R. Lankester. "On the coincidence of the blastopore and anus in Paludina vivipara." Quart. J. of Micr. Scie., Vol. XVI. 1876.
(264) F. Leydig. "Ueber Paludina vivipara." Zeitschr. f. w. Zool., Vol. 11. 1850.
(265) J. MUller. Ueber Synapta dig. u. iib. d. Erzeug. v. Schnecken in Holoth., 1852.
(266) J. Miiller. "Bemerk. aus d. Entwickl. der Pteropoden." Monatsber. Berl. Akad., 1857.
(267) C. Rabl. "Die Ontogenie d. Siisswasser-Pulmonaten." Jenaische Zeitschrift, Vol. IX. 1875.
(268) C. Rabl. "Ueb. d. Entwick. d. Tellerschnecke (Planorbis)." Morph. Jahrbuch, Vol. v. 1879.
(269) W. Salensky. " Beitr. zur Entwickl. d. Prosobr." Zeitschr. f. iv. Zool. , Vol. xxii. 1872.
(270) O. Schmidt. "Ueb. Entwick. von Limax agrestis." Miillcr's Archiv, 1851.
(271) Max S. Schultze. "Ueber d. Entwick. des Tergipes lacinulatus." Arch. f. Naturg., Jahrg. XV. 1849.
(272) E. Selenka. "Entwick. von Tergipes claviger." Niederl. Arch.f. Zool., Vol. I. 1871.
(273) E. Selenka. "Die Anlage d. Keimbl. bei Purpura lapillus." Niederl. Arch.f. Zool., Vol. i. 1872.
(274) C. Semper. "Entwickl. der Ampullaria polita, etc." Natuurk. Verhandl. Utrechts Genootsch., 1862.
(275) An. Stecker. "Furchung u. Keimblatterbildung bei Calyptraa." Morphol. Jahrbuch, Vol. n. 1876.
(276) A.Stuart. " Ueb. d. Entwickl. einiger Opisthobr." Zeitschr. f. w. Zool., Vol. XV. 1865.
(277) N. A. Warneck. "Ueber d. Bild. u. Entwick. d. Embryos bei Gasterop." Bullet. Soc. natural, de Moscou, T. xxm. 1850.
(278) P. J. van Beneden. " Recherches sur 1'Embryogenie des Sepioles." Nouv. Mem. Acad. Roy. de Bruxelles, Vol. xiv. 1841.
(279) N. Bobretzky. Observation on the Development of the Cephalopoda (Russian). Nachrichten d. kaiserlichen Gesell. d. Freunde der Naturwiss. Anthropolog. Rthnogr. bei d. Universitdt Moskau.
(280) H. Grenacher. " Zur Entwicklungsgeschichte d. Cephalopoden." Zeit. f. wiss. Zool., Bd. xxiv. 1874.
(281) A. K6 Hiker. Entwicklungsgeschichte d. Cephalopoden. Zurich, 1844.
(282) E. R. Lankester. "Observations on the development of the Cephalopoda." Quart. J. of Micr. Science, Vol. xv. 1875.
(283) E. Metschnikoff. " Le developpement des Sepioles." Archives d. Sc. phys. et nat., Vol. xxx. Geneve, 1867.
(284) A. Kowalevsky. "Ueb. d. Entwick. d. Chitonen." Zoologischer Anzeiger, No. 37. 1879.
(285) S L. Loven. " Om utvecklingen hos sliigtet Chiton." Stockholm ofversigt, xn. 1855. [Vide also Ann. and Mag. of Nat. Hist., Vol. xvii. 1856, ami Archivf. Naturgeschichte, 1856.]
(286) H. Lacaze-Duthiers. "Developpement du Dentale." Ann. d. Sci.
Nat., Series iv. Vol. VII. 1857.
(287) M. Braun. " Postembryonale Entwicklung d. Susswasser-Muscheln."
(288) C. G. Carus. " Neue Untersuch. lib. d. Entvvickl. unscrer FlussmuVcrh. Leop.-Car. Akad., Vol. xvi. 1832.
(289) W. Flemming. " Studien in d. Entwicklungsgeschichte der Najadcn." Sit*, d. k. Akad. Wiss. Wien, Vol. LXXI. 1875.
(290) F. Ley dig. " Ueber Cyclas Cornea." Miiller's Archiv, 1855.
(2111) S. L. Loven. " Bidrag til Kanned. om Utveckl. af Moll. Acephala I^amellibr." Vetensk. Akad. Handl., 1848. [FiVfcalso Arch. f. Naturg., 1849.]
(292) C. Rabl. "Ueber d. Entwicklungsgeschichte d. Malermuschel." Jenaische Zeitschrift, Vol. X. 1876.
(293) W. Salensky. " Bemerkungen uber Haeckels Gastraea-Theorie (Ostrea)." Arch. f. Naturg., 1874.
(294) O. Schmidt. " Ueb. d. Entwick. von Cyclas calyculata." Muller's Arch., 1854.
(295) O. Schmidt. "Zur Entwickl. der Najaden." Wien. Sitzungsber. math.-nat. C!., Vol. xix. 1856.
(296) P. Stepanoff. " Ueber die Geschlechtsorgane u. die Entwicklung von Cyclas." Archivf. Naturgeschichte, 1865.
(297) H. Lacaze-Duthiers. " Ueveloppement d. branchies d. Mollusques Acephales." An. Sc. Nat., Ser. iv. Vol. v. 1856.
(298) J. Barrois. Recherches sur Cembi yologie des Bryozoaires. Lille, 1877.
(299) B. Hatschek. " Embryonalentwicklung u. Knospung d. Pedicellina echinata." Zeitschrift fiir wiss. Zool., Bd. xxix. 1877.
(300) M. Salensky. " Etudes sur les Bryozoaires entoproctes." Ann. Scien. Nat., Ser. vi. Tom. v. 1877.
(301) O. Schmidt. "Die Gattung Loxosoma." Archivf. mik. Anat.,Rd. xii. 1876.
(302) C. Vogt. "Sur le Loxosome des Phascolosomes." Archives de Zool. cxptr. et gtnfr., To.n. v. 1876.
(303) C. Vogt. "Bemerkungen zu Dr Hatschek's Aufsatz lib. Embryonalentwicklung u. Knospung von Pedicellina echinata." Zeit. f. wiss. Zool., Bd. XXX. 1878.
(304) G. J. A 11 man. Monograph of fresh water Polyzoa. Ray Society.
(305) G. J. Allman. " On the structure of Cyphonautes." Quart. J. of Micr. Scie., Vol. xii. 1872.
(306) G. J. Allman. "On the structure and development of the Phylactola> matous Polyzoa." Journal of the Linnean Society, Vol. xiv. No. 77. 1878.
(307) J. Barrois. " Le developpement d. Bryozoaires Chilostomes." Comptes rendus, Sept. 23, 1878.
(308) E. Claparede. " Beitrage zur Anatomic u. Entwicklungsgeschichte d. Seebryozoen." Zeit. fiir wiss. Zool., Bd. xxi. 1871.
(309) E. Claparede. "Cyphonautes." Anat. u. Entwick. wirbell. Thiere. Leipzig, 1864.
(310) R. E. Grant. "Observations on the structure and nature of Flustrae." Edinburgh New Philosoph. Journal, 1827.
(311) B. Hatschek. "Embryonalentwicklung u. Knospung d. Pedicellina echinata" (Description of Cyphonautes). Zeit. f. wiss. Zool., Bd. xxix. 1877.
(312) T. II. Huxley. "Note on the reproductive organs of the Cheilostome Polyzoa." Quart. Jour, of Micr. Science, Vol. IV. 1856.
(313) L. Joliet. "Contributions a 1'histoire naturelle des Bryozoaires des cotes de France." Archives ie Zoologic Experimental, Vol. VI. 1877.
(314) E. Metschnikoff. " Ueber d. Metamorphose einiger Seethiere." Gottingische Nachrichten, 1869.
(315) E. Metschnikoff. Bull. deTAcad. de St Pttersbourg, XV. 1871, p. 507.
(316) H. Nitsche. " Beitrage zur Kenntniss d. Bryozoen." Zrit. f. wiss.
Zool., Bd. xx. 1870.
(317) W. Repiachoff. "Zur Naturgeschichte d. chilostomen Seebryozoen." Zeit.f. wiss. Zool., Bd. xxvi. 1876.
(318) W. Repiachoff. " Ueber die ersten Entwicklungsvorgange bei Tendra zostericola. Zeit. f. wiss. Zoo!., Bd. xxx. 1878. Supplement.
(319) W. Repiachoff. "Zur Kenntniss der Bryozoen." Zoologischer Anzeiger, No. 10, Vol. i. 1878.
(320) W. Repiachoff. " Bemerkungen lib. Cyphonautes. " Zoologischer Anzeiger, Vol. n. 1879.
(321) M. Salensky. " Untersuchung an Seebryozoen." Zeit. fur wiss. Zool.. Bd. xxiv. 1874.
(322) A. Schneider. "Die Entwicklung u. syst. Stellung d. Bryozoen u. Gephyreen." Archiv f. mikr. Anaf., Vol. v. 1869.
(323) Smitt. " Om Hafsbryozoernas utveckling och fettkroppar. " Aftryck ur ofvers. of Kong. Vet. Akad. Fork. Stockholm, 1865.
(324) T. Hincks. British Marine Polyzoa. Van Voorst, 1880. [Conf. also works by Farre, Hincks, Van Beneden, Dalyell, Nordmann.]
(325) W. K. Brooks. " Development of Lingula." Chesapeake Zoological Laboratory, Scientific Results of the Session of 1878. Baltimore, J. Murphy and Co.
(326) A. Kowalevsky. "Development of the Brachiopoda." Protocol of the First Session of the United Sections of Anatomy, Physiology, and Comparative Anatomy at the Meeting of Russian Naturalists in Kasan, 1873. (Russian.)
(327) H. Lacaze-Duthiers. " Histoire de la Thecidie." Ann. Scien. Nat. etc. Ser. 4, Vol. xv. 1861.
(328) Morse. " On the Early Stages of Terebratulina septentrionalis." Mem. Boston Soc. Nat. History, Vol. n. 1869, also Ann. &> Mag. of Nat. Hist. Series 4, Vol. vm. 1871.
(329) Morse. "On the Embryology of Terebratulina." Mem. Boston Soc. Nat. History, Vol. ill. 1873.
(330) Morse. " On the Systematic Position of the Brachiopoda." Proceedings of the Boston Soc. of Nat. Hist., 1873.
(331) Fritz Miiller. " Beschreibung einer Brachiopoden-Larve." Miiller's Archiv, 1860.
(332) Alex. Agassiz. "On the young stages of a few Annelids." Annals Lyceum Nat. Hist, of New York, Vol. vm. 1866.
(333) Alex. Agassiz. " On the embryology of Autolytus cornutus and alternations of generations, etc." Boston Journal of Nat. History, Vol. VH. 1859-63.
(334) W. Busch. Beobachtungen it. Anaf. u. Entwick. einiger wirbelloser Seethiere, 1851.
(335) Ed. Claparede. Beobachtungen u. Anat. u. Entwick. 'wirbelloser Thiert an d. Kiiste von Normandie. Leipzig, 1 863.
(336) Ed. Claparede u. E. Metschnikoff. "Beitrage z. Kenntniss lib. Entwicklungsgeschichte d. Chsetopoden." Zeit.f. wiss. Zool., Vol. xix. 1869.
(337) E. Grube. Untersuchungen ub. Entivicklung d. Anneliden. Komgsberg,
4 (338) B. Hatschek. " Beitrage z. Entwick. u. Morphol. d Anneliden." Si/*. d. k. Akad. Wiss. Wien, Vol. LXXIV. 1876.
(339) B. Hatschek. "Studien liber Entwicklungsgeschichte der Anneliden. Arbeiten aus d. zoologischcn Institute d. Universitiit Wien. Von C. Claus. Heft in.
(340) Th. H. Huxley. "On hermaphrodite and fissiparous species of tubicolar Annelidse (Protula)." Edinburgh New Phil. Journal, Vol. I. 1855.
(341) N. Kleinenberg. "The development of the earthworm Lumbncus trapezoides." Quart. J, of Micr. Science, Vol. xix. 1879 Sullo ariAtfff del tn<
bricus trapezoides. Napoli, 1878.
(342) A. Kowalevsky. " Embryologische Studien an Wiirmern u. Arthropoden." Mem. Acad. Pttersbourg, Series VH. Vol. xvi. 1871.
(343) A. Krohn. " Ueber die Erscheinungen bei d. Fortpfianzung von Syllis prolifera u. Autolytus prolifer." Archiv f. Naturgesch. 1852.
(344) R. Leuckart. " Ueb. d. Jugendzustande ein. Anneliden, etc." Archiv f. Naturgesch. 1855.
(345) S. Love"n. " Beobachtungen ii. die Metamorphose von Anneliden." Wiegmann's Archiv, 1842.
(346) E. Metschnikoff. "Ueber die Metamorphose einiger Seethiere (Mitraria)." Zeit.f. tuiss. Zool., Vol. XXI. 1871.
(347) M. Milne- Ed\vards. " Recherches zoologiques, etc." Ann. Scie. Natur. HI. Se"rie, Vol. ill. 1845.
(348) J. Miiller. "Ueb. d. Jugendzustande einiger Seethiere." Monats. d. k.Akad. Wiss. Berlin, 1851.
(349) Max Miiller. "Ueber d. weit. Entwick. von Mesotrocha sexoculata." Miiller's Archiv, 1855.
(350) Quatrefages. " Memoire s. 1'embryogenie des Annelides." Ann. Scie. Natur. HI. Serie, Vol. x. 1848.
(351) M. Sars. " Zur Entwicklung d. Anneliden." Archiv f. Naturgeschichte, Vol. xi. 1845.
(352) A. Schneider. " Ueber Bau u. Entwicklung von Polygordius." Miiller's Archiv, 1868.
(353) A. Schneider. "Entwicklung u. system. Stell. d. Bryozoen u. Gephyreen (Mitraria)." Archiv f. mikr. Anat. Vol. v. 1869.
(354) M. Schultze. Ueb. die Entwicklung von Arcnicola piscatorum u. anderer Kiemenwurmer. Halle, 1856.
(355) C. Semper. "Die Verwandschaftbeziehungen d. gegliederten Thiere." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. in. 1876-7.
(356) C. Semper. "Beitrage z. Biologie d. Oligochjeten." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. IV. 1877-8.
(357) M. Stossich. " Beitrage zur Entwicklung d. Chaetopoden." Sitz. d. k. k. Akad. Wiss. Wien, B. LXXVII. 1878.
(358) R. v. Willemoes-Suhm. " Biologische Beobachtungen ii. niedrige Meeresthiere." Zeit.f. wiss. Zool. Bd. xxi. 1871.
(359) O. BUtschli. " Entwicklungsgeschichtliche Beitrage (Nephelis)." Zeit. f. wiss. Zool. Vol. xxix. 1877.
(360) E. Grube. Untersuchungen ub. d. Entwicklung d. Anneliden. Konigsberg, 1844.
(361) C. K. Hoffmann. "Zur Entwicklungsgeschichte d. Clepsineen." NICderland. Archiv f. Zool. Vol. IV. 1877.
(362) R. Leuckart. Die menschlichen Parasiten (Hirudo}, Vol. I. p. 686, et seq.
(363) H. Rathke. Beit. z. Entwicklungsgesch. d. Hirudineen. Leipzig, 1862.
(364) Ch. Robin. Mem. snr le Developpement embryogenique des Ilirndiih'c*. Paris, 1875.
(365) C. O. Whitman. "Embryology of Clepsine." Quart. J. of Micro. Science, Vol. xvm. 1878.
[ Vide also C. Semper (No. 355) and Kowalevsky (No. 342) for isolated observations.]
GEPHYREA. GepJiyrea nuda.
(366) A. Kowalevsky. Sitz. d. zool. Abth. d. Iff. Versam. rtiss. Naturf (Thalassema). Zeit.f. wiss. Zool. Vol. xxn. 1872, p. 284.
(367) A. Krohn. "Ueb. d. Larve d. Sipunculus nudus ncbst I'.c UK iknii^cn, ' etc. Miiller's Archiv, 1857.
(368) M. Salensky. " Ueber die Metamorphose d. Echiurus." Morfhohgisches Jahrbuch, Bd. 11.
(369) E. Selenka. "Eifurchung u. Larvenbilflung von Phascolosoma elongatum." Zeit.f. wiss. Zool. 1875, Bd- xxv. p. i.
(370) J. W. Spengel. " Beitrage z. Kenntniss d. Gephyreen (lionellia)." MitlheiL a. d. zool. Station z. Neapel, Vol. i. 1879.
Gephyrea tubicola (Actinotroc/ia).
(371) A. Krohn. " Ueb. Pilidium u. Actinotrocha." Muller's Archiv, 1858.
(372) A. Kowalevsky. " On anatomy and development of Phoronis," Petersburg, 1867. i PI. Russian. Vide Leuckart's Bcricht, 1866-7.
(373) E. Metschnikoff. " Ueber d. Metamorphose einiger Seethiere (Actinotrocha)." Zeit.f. wiss. Zool. Bd. XXI. 1871.
(374) J. Miiller. " Bericht ub. ein. Thierformen d. Nordsee." Muller's Archiv, 1846.
(375) An. Schneider. "Ueb. d. Metamorphose d. Actinotrocha branchiata." Muller's Arch. 1862.
(376) O. Butschli. " Zur Entwicklungsgeschichte der Sagitta." Zeilschrifl f. wiss. Zool., Vol. xxin. 1873.
(377) C. Gegenbaur. "Ueber die Entwicklung der Sagitta." Abhand. d. natiirforschenden Gesellschaft in Halle, 1857.
(378) A. Kowalevsky. " Embryologische Studien an Wiirmern u. Arthropoden." Mem. Acad. Petersbourg, vn. ser., Tom. xvi., No. 12. 1871.
(379) L.Graff. Das Genus Myzostoma. Leipzig, 1877.
(380) E. Metschnikoff. "Zur Entwicklungsgeschichte d. Myzostomum." Zeit.f. wiss. Zool., Vol. xvi. 1866.
(381) C. Semper. "Z. Anat. u. Entwick. d. Gat. Myzostomum." Zeit.f. wiss. Zool., Vol. IX. 1858.
(382) H. Ludwig. " Ueber die Ordnung Gastrotricha Metschn." Zeit.f. wiss. Zool., Vol. xxvi. 1876.
(383) O. Butschli. "Entwicklungsgeschichte d. Cucullanus elegans." Zeit. f. wiss. Zool., B. xxvi. 1876.
(384) T. S. Cobbold. Entozoa. Groombridge and Son, 1864.
(385) T. S. Cobbold. Parasites; a Treatise on the Entozoa of Man and Animals. Churchill, 1879.
(386) O. Caleb. "Organisation et developpement des Oxyurides, etc. Archives de Zool. exper. et gener., Vol. VII. 1878.
(387) R. Leuckart. Untersuchungeniib. Trichina spiralis. 2nd ed. Leipzig, 1866.
(388) R. Leuckart. Die menschlichen Parasiten, Bd. u. 1876.
(389) H. A. Pagenstecher. Die Trichinen nach Versuchen dargestellt.
(390) A.Schneider. Monographie d. Nematoden. Berlin, 1866.
(391) A. Villot. " Monographie des Dragoneaux " (Gordioidea). Archives de Zool. exptr. et gtner., Vol. in. 1874.
(392) R. Greeff. " Untersuchungen u. d. Ban u. Entwicklung des Echin. miliarius." Archiv f. Naturgesch. 1864.
(393) R. Leuckart. Die menschlichen Parasiten. Vol. 11. p Soi ol
(394) An. Schneider. " Ueb. d. Bau d. Acanthocephalen." Archiv f. Anat. w. Phys. 1868.
(395) G. R. Wagener. Beitrdge z. Entrvicklungsgeschichte d. Eingeweidewiirmer. Haarlem, 1865.
PRO TO TRA CHE A TA .
(396) H. N. Moseley. "On the Structure and Development of Peripatus capensis." Phil. Trans. Vol. 164, 1874.
(397) G. Newport. "On the Organs of Reproduction and Development of the Myriapoda." Philosophical Transactions, 1841.
(398) E. Metschnikoff. " Embryologie der doppeltfiissigen Myriapoclen (Chilognatha)." Zeit.f. wiss. Zool., Vol. xxiv. 1874.
(399) E. Metschnikoff. " Embryologisches iiber Geophilus." Zeit. f. wiss. 'Zool., Vol. xxv. 1875.
(400) Anton Stecker. "Die Anlage d. Keimblatter bei den Diplopoden." Archiv f. mik. Anatomic, Bd. xiv. 1877.
(401) M Balbiani. " Observations s. la reproduction d. Phylloxera du Chene." An. Sc. Nat. Ser. v. Vol. xix. 1874.
(402) E. Bessels. "Studien u. d. Entwicklung d. Sexualdrtisen bei den Lepidoptera." Zeit.f. miss. Zool. Bd. xvn. 1867.
(403) Alex. Brandt. " Beitrage zur Entwicklungsgeschichte d. Libellulida u. Hemiptera, mit besonderer Beriicksichtigung d. Embryonalhiillen derselben." Mem. Ac. Pttersbourg, Ser. vn. Vol. xin. 1869.
(404) Alex. Brandt. Ueber das Ei u. seine Bildungsstdtte. Leipzig, 1878.
(405) O. Butschli. " Zur Entwicklungsgeschichte d. Biene." Zeit. f. wiss. Zool. Bd. xx. 1870.
(406) H. Dewitz. "Bau u. Entwicklung d. Stachels, etc." Zeit.f. wiss. Zool. Vols. xxv. and xxvin. 1875 and 1877.
(407) H. Dewitz. "Beitrage zur Kenntniss d. Postembryonalentwicklung d. Gliedmassen bei den Insecten." Zeit. /. wiss. Zool. xxx. Supplement. 1878.
(408) A. Dohrn. "Notizen zur Kenntniss d. Insectenentwicklung." Zeitschriftf. wiss. Zool. Bd. xxvi. 1876.
(409) M. Fabre. " L'hypermetamorphose et les mceurs des Meloides." An. Sci. Nat. Series iv. Vol. vn. 1857.
(410) Ganin. "Beitrage zur Erkenntniss d. Entwicklungsgeschichte d. Insecten." Zeit. f. wiss. Zool. Bd. xix. 1869.
(411) V. Graber. Die Insecten. Miinchen, 1877.
(412) V. Graber. " Vorlauf. Ergeb. lib. vergl. Embryologie d. Insecten." Archiv f. mikr. Anat. Vol. XV. 1878.
(413) O.v.Grimm. " Ungeschlechtliche Fortpflanzung einer Chironomus-Art u. deren Entwicklung aus dem unbefruchteten Ei." Mhn. Acad. Pttcrsbourg. 1X70.
(414) B. Ilatschek. " Beitrage zur Entwicklung d. Lepidopteren." Jenaischc Zeitschrift, Bd. xi.
(415) A. Kollikcr. " Observationes de prima insectorum gcnese, etc. " Ann. Sc. Nat. Vol. xx. 1843.
(11(5) A. Kowalevsky. " Embryologische Studien an Wiirmern u. Arthropoden." Mtm. Ac. imp. J\'(,-rstn>nr, Ser. VII. Vol. XVI. iSji.
(417) C. Kraepelin. " Untersuchungen lib. d. Bau, Mechanismus u. d. Entwick. des Stachels d. l.icnartigai Tliicrc." Zeit.f. wiss. Zool. Vol. xxm. 1X7.5.
(418) C. Kupffcr. " Faltcnblatt nn d. Embryoncn d. Gattung Chirononnis." Arch.f. mikr. Anat. Vol. n. iS66.
(419) R. Leuckart. Zur Kemituiss d. Gi'ncratiomxi'ffhscls it. d. /'/; -Ihetii^ , < b. d. Insecten. Frankfurt, iH.nS.
(420) Lubbock. Origin and Metamorphosis of Insi-cts. 1874.
(421) Lubbock. Monograph on Collembola ami Thysanura. Ray Society, 1873 (422) Melnikow. " Beitrage z. Embryonalentwicklung d. Insecten." Archiv f. Naturgeschichte, Bd. XXXV. 1869.
(423) E. Metschnikoff. ' ' Embryologische Studien an Insecten." '/.fit. /. wiss. Zool Bd. xvi. 1866.
(424) P. Meyer. " Ontogenie und Phylogenie d. Insecten." Jcnaischt Zfitschrift, Vol. X. 1876.
(425) Fritz Miiller. " Beitrage z. Kenntniss d. Termiten." Jcnaische Zeitschrift, Vol. IX. 1875.
(426) A. S. Packard. " Embryological Studies on Diplex, Perithemis, and the Thysanurous genus Isotoma." Mem. Pea body Acad. Science, \. 2. 1871.
(427) Suckow. " Geschlechtsorgane d. Insecten." Heusinger's Zeitschrift f. organ. Physik, Bd. II. 1828.
(428) Tichomiroff. " Ueber die Entwicklungsgeschichte des Seidenwiirms." Zoologischer Anzeigcr, n. Jahr. No. 20 (Preliminary Notice).
(429) Aug. Weismann. "Zur Embryologie d. Insecten." Arehiv f. Anat. und Phys. 1864.
(430) Aug. Weismann. " Entwicklung d. Dipteren." Zeit. f. wiss. Zool. Vols. xni. and xiv. Leipzig, 1863 4.
(431) Aug. Weismann. " Die Metamorphose d. Corethra plumicornis." Ztit. f. unss. Zool. Vol. xvi. 1866.
(432) N. Wagner. " Beitrag z. Lehre d. Fortpflanzung d. Insectenlarven." Zeit.f. wiss. Zool. Vol. Xlll. 1860.
(433) Zaddach. Untersuchnngen tib. d. Bau u. d. Enhuicklung d. Gliederlhifre. Berlin, 1854.
ARACHNID A. Scorpionidce.
(434) El. Metschnikoff. " Embryologie des Scorpions." Zeit.f. unss. Zool. Bd. xxi. 1870.
(435) H. Rathke. Reisebemerknngen aus Taurien (Scorpio), Leipzig, 1837.
(436) El. Metschnikoff. " Entwicklungsgeschichte d. Chelifer." Zeit.f. unss. Zool. Bd. xxi. 1870.
(437) A. Stecker. "Entwicklung der Chthonius-Eier im Mutterleibe und c Bildung des Blastoderms." Sitzung. konigl. bohmisch. Gesellschaft Wissensch. t 1876, 3. Heft, and Annal. and Mag. Nat. History, 1876, xvill. 197.
(438) M. Balbiani. " Memoire sur le developpement des Phalangides." Ann. Scien. Nat. Series v. Vol. xvi. 1872.
(439) M. Balbiani. "Memoire sur le developpement des Araneides." Ann. Scien. Nat. Series v. Vol. xvn. 1873. /->./
(440) F. M. Balfour. "Notes on the development of the Arane
Journ. of Micr. Science, Vol. XX. 1880. v ,
(441) J. Barrois. " Recherches s. 1. developpement des Araign^es.
de I' Anat. et de la Physiol. 1878. , , fiA
(442) E. Claparede. Recherches s. revolution des Aratgnees. Jtrecht, 1862.
(443) Her old. De generation Araneorum in Ovo. Marburg, 1824.
(444) H. Ludwig. "Ueber die Bildung des Blastoderms bei den Zeit.f. wiss. Zool. Vol. xxvi. 1876.
B. II. b
(445) P. van Beneden. " Developpement de 1'Atax ypsilophora." Acad. Bruxelles, t. xxiv.
(446) Ed. Claparede. "Studien uber Acarinen." Zeit. /. wits. Zoo/., Bd. xvin. 1868.
CRUSTACEA. General Works.
(447) C. Spence Bate. " Report on the present state of our knowledge of the Crustacea." Report of the British Association for 1878.
(448) C. Claus. Untersuchungen zur Erforschung der genealogischen Grundlage des Crustaceen -Systems. Wien, 1876.
(449) A. Dohrn. "Geschichte des Krebsstammes. " Jenaische Zeitschrift, Vol. vi. 1871.
(450) A. Gerstaecker. Bronris Thierreich, Bd. v. Arthropoda, 1866.
(451) Th. II. Huxley. The Anatomy of Invertebrated Animals. London, 1877.
(452) Fritz Miiller. Fiir Darwin, 1864. Translation, Facts for Darwin. London, 1869.
(453) Brauer. "Vorlaufige Mittheilung iiber die Entwicklung u. Lebensweise des Lepidurus (Apus) productus." Sitz. der Ak. d. Wiss. Wien, Vol. LXIX., 1874.
(454) C. Claus. ' Zur Kenntniss d. Baues u. d. Entwicklung von Branchipus stagnalisu. Apuscancriformis." Abh. d. konig. Gesell. der Wiss. Gbttingen, Vol. xviii.
(455) C. Grobben. "Zur Entwicklungsgeschichte d. Moina rectirostris." Arbeit, a. d. zoologisch. Institute Wier., Vol. II., 1879.
(456) E. Grube. " Bemerkungen iiber die Phyllopoden nebst einer Uebersicht etc." Archivf. Naturgcschichte, Vol. xix., 1853.
(457) N. Joly. " Histoire d'un petit Crustace (Artemia salina, Leach) etc." Annales d. Sciences Natur., 2nd ser., Vol. xiir., 1840.
(458) N. Joly. " Recherches zoologiques anatomiques et physiologiques sur 1' I sauracy clad oides ( = Esther ia) nouveau genre, etc." Annales d. Sciences Nat., 2nd ser., Vol. xvii., 1842.
(459) Lereboullet. " Observations sur la generation et le de veloppement de la Limnadia de Hermann." Annales d. Sciences Nattir., ^th ser., Vol. v., 1866.
(460) F. Ley dig. " Ueber Artemia salina u. Branchipus stagnalis." Zeit. f. wiss. Zool., Vol. in., 1851.
(461) G. O. Sars. "Om en dimorph Udvikling samt Generationsvexel hos I^eptodora." Vidensk. Selskab. For hand, 1873.
(462) G. Zaddach. De apodis cancrefortnis Schaeff. anatome ct historia evolutionis. Dissertatio inanguralis zootomica. Bonnae, 1841.
(463) C. Claus. " Ueber den Bau u. die systematische Stellung von Nebalia." Zeit.f. wiss. Zool., 15d. xxn. 1872.
(464) E.Metschnikoff. Development of Nebalia ( Russian), 1 868.
(465) E. van Beneden. "Recherches sur 1'Embryogenie des Crustace's. u. Developpement des Mysis." liullet. de rAcadc ! mie roy. de Belgique, second series, Tom. xxvin. 1869.
(46H) C. Claus. " Ueber einige Schizopoden u. niedere Malakostraken." Zeit. /. -t'tss. Zoologie, Bd. XIII., 1863.
(467) A. Dohrn. " Untersuchungen iib. Bau u. Entwicklung d. Arthropoden." Zeit. f. wiss. Zool., Bd. xxi., 1871, p. 375. Peneus zoaea (larva of Euphausia).
(468) E. Metschnikoff. " Ueber ein Larvenstadium von Euphausia." Zeit. fiir wiss. Zool., Bd. xix., 1869.
(469) E. Metschnikoff. " Ueber den Naupliuszustand von Euphausia." Zeit. fiir wiss. Zool., Bd. xxi., 1871.
(470) Spence Bate. "On the development of Decapod Crustacea." Phil. Trans., 1858.
(471) Spence Bate. " On the development of Pagurus." Ann. and Mag. Nat. History, Series 4, Vol. 1 1., 1868.
(472) N. Bobretzky. Development of Astacus and Paluemon. Kiew, 1873. (Russian.)
(473) C. Claus. "Zur Kenntniss d. Malakostrakenlarven." Wiirzb. naturw. Zeitschrift, 1861.
(474) R. Q. Couch. "On the Metamorphosis of the Decapod Crustaceans." Report Cornwall Polyt. Society, 1848.
(475) Du Cane. "On the Metamorphosis of Crustacea." Ann. and Mag. of Nat. History, 1839.
(476) Walter Faxon. " On the development of Paloemonetes vulgaris." Bull. of the Mus. of Comp. Anat. Harvard, Cambridge, Mass., Vol. V., 1879.
(477) A. Dohrn. " Untersuchungen iib. Bau u. Entwicklung d. Arthropoden." " Zur Entwicklungsgeschichte der Panzerkrebse. Scyllarns Palinurus." Zeit. f. wiss. Zool., Bd. xix., 1870.
(478) A. Dohrn. "Untersuchungen iib. Bau u. Entwicklung d. Arthropoden. Erster Beitrag z. Kenntniss d. Malacostrakcn u. ilirer Larven Amphion Reynaudi, Lophogaster, Portunus, Porcellanus, Elaphocaris. " Zeit. f. ^viss. Zool., Bd. XX., 1870.
(479) A. Dohrn. "Untersuchungen iib. Bau u. Entwicklung d. Arthropoden. Zweiter Beitrag, etc." Zeit.f. wiss. Zool., Bd. XXI., 1871.
(480) N. J oly. " Sur la Caridina Desmarestii." Ann. Scien. Nat., Tom. xix., 1843.
(481) Lereboullet. " Recherches d. 1'embryologie comparee sur le developpement du Brochet, de la Perche et de 1'Ecrevisse." Mem. Savuns Etrang. Paris, Vol. xvii., 1862.
(482) P. Mayer. "Zur Entwicklungsgeschichte d. Dekapoden." Jenaische Zeitschrift, Vol. XI., 1877.
(483) Fritz Miiller. '* Die Verwandlung der Porcellana." Archivf. Naturgeschichte, 1862.
(484) Fritz Miiller. " Die Verwandlungen d. Garneelen." Archivf. Naturgesch., Tom. xxix.
(485) Fritz Miiller. " Ueber die Naupliusbrut d. Garneelen." Zeit. f. wiss. Zool., Bd. xxx., 1878.
(486) T. J. Parker. "An account of Reichenbach's researches on the early development of the Fresh-water Crayfish." Quart. J. of M. Science, Vol. xvui., 1878.
(487) H. Rathke. Ueber die Bildung u. Entwicklung d. Flusskrebses. Leipzig, 1829.
(488) H. Reichenbach. " Die Embryoanlage u. erste Entwicklung d. Flusskrebses." Zeit. f. wiss. Zool., Vol. xxix., 1877.
(489) F. Richters. "Ein Beitrag zur Entwicklungsgeschichte d. Loricaten." Zeit.f. wiss. Zool., Bd. xxiii., 1873.
(490) G. O. Sars. " Om Hummers postembryonale Udvikling." Vidcnsk Selsk. Forh. Christiania, 1874.
(491) Sidney J. Smith. " The early stages of the American Lobster. " Tratts. of the Connecticut Acad. of Arts and Sciences, Vol. II., Part i, 1873.
(492) R. v. Willemoes Suhm. " Preliminary note on the development of some pelagic Decapoda." Proc. of Royal Society, 1876.
(41KI) \V. K. Brooks. " On the larval stages of Squilla empusa. Chesapeake Zoological Laboratory^ Scientific results of the Session ^1878. Baltimore, 1879.
(494) C. Claus. "Die Metamorphose der Squilliden." Abhand. dcr konigl. Gesell. der IViss. ztt Gottingen^ 1*7-.
( 1 '.!">) Fr. M tiller. 4i Bruchstuck a. der Entwicklungsgeschichte d. Maulfiisser I. und II." Archivf. Naturgeschichte, Vol. xxvni., 1862, and Vol. XXIX., 1863.
( 1%) A. Dohrn. " Ueber den Bau u. Entwicklung d. Cumaceen." Jenaische Zeitschrift, Vol. v., 1870.
(497) Ed. van Beneden. " Recherches sur 1'Embryogenie des Crustaces. i. Asellus aquaticus." BiuL de FAcad. roy. Belgique, 2me serie, Tom. XXVIII., No. 7, 1869.
(498) N. Bobretzky. "Zur Embryologie des Oniscus murarius." Ztit. fur wiss. Zool., Bd. xxiv., 1874.
(4119) J. F. Bullar. "On the development of the parasitic Isopoda." Phil. Trans., Part n., 1878.
(500) A. Dohrn. " Die embryonale Entwicklung des Asellus aquaticus." Zeit. f. wiss. Zool., Vol. xvii., 1867.
(501) II. Rathke. Untersuchungen iibcr die Bildung und Entwicklung der VVasser-Assel. Leipzig, 1832.
(5u2) H. Rathke. Zur Morphologic. Reisebemerkungen aus J^aurien. Riga u. Leipzig, 1837. (Bopyrus, Idothea, Ligia, lanira.)
. A mphipoda.
(503) Ed. van Beneden and E. Bessels. "Memoire sur la formation du blastoderme chez les Amphipodes, les Lerneens et les Copepodes." Classe des Sciences de F Acad. roy. de Belgiqtie, Vol. xxxiv., 1868.
(004) De la Valette St George. " Studien liber die Entwicklung der Amphipoden." Abhand. d. naturfor. Gesell. zu Halle, Bd. v., 1860.
(505) E. van Beneden and E. Bessels. "Memoire sur la formation du blastoderme chez les Amphipodes, les Lerneens et Copepodes." Classe des Sciences dc FAcad. roy. de Bel^ique, Vol. xxxiv., 1868.
(">(Hi) E. van Beneden. " Recherches sur 1'Embryoge'nie des Crustaces I v. Anchorella, Lerneopoda, Branchiella, Hessia." Bull, de FAcad. roy. de Belgique^ sme serie, T. xxix., 1870.
(507) C. Claus. Zur Anatomie u. Entwicklungsgeschichte d. Copepoden.
("iii.S) C. Claus. " Untcrsuchungen iiber die Organisation u. N'crwaiulschaft d. Copepoden." Witrzburger nalttnviss. Zeitschrift, Bd. ill., 1862.
(.")('.() C. Claus. ' Ueber den Bau u. d. Entwicklung von Achtheres percarum." '/.cit.f. wiss. Zool., Bd. XI., 1862.
I ."> 1 ( i ) C . (' 1 a u s. Die frcilcbcnden Copepoden mit bcsonderer Beritcksichtigiing der Fauna Dcutschlands, der Nordsec u. des Mitteltnecres. Leip/.i.^, 1863.
(511) C. C laus. " Ueber d. Entwicklung, Organisation u. systematische Stellung d. Arguliihv." /.eit. f. wiss. tool., P>d. xxv., 1875.
(51^) P. P. C. Hoek. "Zur Entwicklungsgeschichte d. Entomostracen." Niederliindischcs Archiv, Vol. IV., 1877.
(513) N o rd m a n n. Mikrographische Beitrdge zur Naturgeschichte der ivirbcllosen Thiert Z\\ cites Heft. 1832.
|.">M) Salensky. " Sphseronella Leuckartii." Archivf. Naturgcschichtc, 1868.
(515) F. Vejdovsky. "Untersuchnngen lib. d. Anat. u. Mctamorph. v. Trachcliastes polycolpus " Zcit.f. wiss. Zool., Vol. xxix., 1877.
(516) C. Spence Bate. "On the development of the Cirripedia." Annals and Mag. of Natur. History. Second Series, vm., 1851.
(517) E. van Beneden. " Developpement des Sacculines." Bull, de F Acad. roy. de Belg., 1870.
(518) C. Claus. Die Cypris-dhnliehe Larve der Cirripedien. Marburg, 1869.
(519) Ch. Darwin. A monograph of the sub-class Cirripedia, i Vols., Kay Society, 1851 4.
(520) A. Dohrn. " Untersuchungen iibcr Bau u. Entwicklung d. Arthropoden ix. Eine neue Naupliusform (Archizoea gigas)." Zeit. f. wiss. Zool., Bd. XX., 1870.
(521) P. P. C. Hoek. "Zur Entwicklungsgeschichte der Entomostraken I. Embryologie von Balanus." Wiederlandisches Archiv fur Zoologic, Vol. III., 1876 7.
(522) R. Kossmann. " Suctoria u. Lepadidze. Arbeiten a. d. zool.-zoot. Instituted. Univer. Wiirz., Vol. I., 1873.
(523) Aug. Krohn. " Beobachtungen iiber die Entwicklung der Cirripedien." Wiegmanrfs Archiv fur Naturgesch., xxvi., 1860.
(524) E. Metschnikoff. Sitzungsberichte d. Versammlung deutscher Naturforscher zu Hannover ; 1865. (Balanus balanoides.)
(525) Fritz Muller. "Die Rhizocephalen." Archiv /. Naturgeschichte, 18623.
(526) F. C. Noll. "Kochlorine hamata, ein bohrendes Cirriped." Zeit.f. wiss. Zool., Bd. xxv., 1875.
(527) A. Pagenstecher. " Beitrage zur Anatomic und Entwicklungsgeschichte von Lepas pectinata." Zeit.f. wiss. Zoo/., Vol. xin., 1863.
(52tt) J. V. Thompson. Zoological Researches and Illustrations, Vol. I., Part I. Memoir iv. On the Cirripedes or Barnacles. 8vo. Cork, 1830.
(529) J. V. Thompson. " Discovery of the Metamorphosis in the second type of the Cirripedes, viz. the Lepades completing the natural history of these singular animals, and confirming their affinity with the Crustacea." Phil. Trans. 1835. P art n.
(530) R. von Willemoes Suhm. "On the development of Lepas fascicularis." Phil. Trans., Vol. 166, 1876.
(531) C. Claus. " Zur naheren Kenntniss der Jugendformen von Cypris ovum." Zeit.f. wiss. Zool., Bd. XV., 1865.
(532) C. Claus. "Beitrage zur Kenntniss d. Ostracoden. Entwicklungsgeschichte von Cypris ovum." Schriften d. Gesell. zur Bejorderung d. gesamm. Naturwiss. zu Marburg, Vol. IX., 1868.
(533) A. Dohrn. "Untersuch. lib. Bau u. Entwick. d. Arthropoden (Limulus polyphemus)." Jcnaische Zeitschrift, Vol. VI., 1871.
(534) A. S. Packard. "The development of Limulus polyphemus." Mem. Boston Soc. Nat. History, Vol. II., 1872.
(535) G. C a van n a. " Studie e ricerche sui Picnogonidi." PiMIicazioni del R. Instittito di Studi super iori in Firenze, 1877.
(536) An. Dohrn. " Ueber Entwicklung u. Bau d. Pycnogoniden." Jenaische Zeitschrift, Vol. v. 1870, and "Neue Untersuchungen ub. Pycnogoniden." Mittheil. a. d. zoologischen Station zu Ncapel, Bd. I. 1878.
(537) G. Hodge. " Observations on a species of Pycnogon, etc." Annal. and Mag. of Nat. Hist. Vol. ix. 1862.
(538) C. Semper. " Ueber Pycnogoniden u. ihre in Hydroiden schmarotzenden Larvenformen. 1 ' Arbeiten a. d. zool.-zoot. Instit. IViiizburg, Vol. I. 1874.
(539) P. T. van Ben e den. " Recherches s. 1'organisation et le developpement d. Linguatules. Ann. d. Scien. Nat., 3 Ser., Vol. XI.
("I'M R. Leuckart. " Bau u. Entwicklungsgeschichte d. Pentastomen." Leipzig and Heidelberg. 1860.
(541) J. Kaufmann. " Ueber die Entwicklung u. systematische Stellung d. Tardigraden." Zeit.f. iviss. Zool., Bd. ill. 1851.
(542) Alex. Agassiz. Revision of the Echini. Cambridge, U.S. 1872 74.
(543) Alex. Agassiz. " North American Starfishes." Memoirs of the Museum of Comparative Anatomy and Zoology at Harvard College, Vol. v., No. i. 1877 (originally published in 1864).
(544) J. Barrois. " Embryogenie de 1'Asteriscus verruculatus " Journal de VAnat. et Phys. 1879.
(545) A. Baur. Beitrdge zur Naturgeschichte d. Synapta digitata. Dresden, 1864.
(546) H. G. Bronn. Kiassen u. Ordnungen etc. Strahlenthiere, Vol. II. 1860.
(547) W. B. Carpenter. "Researches on the structure, physiology and development of Antedon." Phil. Trans. CLVI. 1866, and Proceedings of the Roy. Soc., No. 166. 1876.
(548) P. H. Carpenter. " On the oral and apical systems of the Echinoderms." Quart. J. of Micr. Science, Vol. xvni. and xix. 1878 9.
(549) A. Gotte. " Vergleichende Entwicklungsgeschichte d. Comatula mediterranea." Arch.fiir micr. Anat., Vol. xn. 1876.
(550) R. Greeff. "Ueber die Entwicklung des Asteracanthion rubens vom Ei bis zur Bipinnaria u. Brachiolaria." Schriftcn d. Gesellschaft zur Beforderung d. gesarnmlen Natnrwissenschaften zu Marburg, Bd. XII. 1876.
(551) R. Greeff. "Ueber den Bau u. die Entwicklung d. Echinodermen." Sitz. d. Gesell. z. Beforderung d. gesam. Naturwiss. zu Marburg, No. 4. 1879.
(552) T. H. Huxley. "Report upon the researches of Mliller into the anat. and devel. of the Echinoderms." Ann. and Mag. of Nat. Hist., 2nd Ser., Vol. vin.
(553) Koren and Danielssen. "Observations sur la Bipinnaria asterigera." Ann. Scien. Nat., Ser. in., Vol. VII. 1847.
i-">l) Koren and Uanielssen. "Observations on the development of the Starfishes." Ann. and Mag. of Nat. Hist., Vol. XX. 1857.
(."..",.",) A. Kowalevsky. "Entwicklungsgeschichte d. Holothurien." Aft m. Ac. Petersburg, Ser. VII., Tom. XI., No. 6.
("'"><') A. Krohn. "Beobacht. a. d. Entwick. d. Holothurien u. Seeigel." M tiller's Archiv, 1851.
(Vi7) A. Krohn. " Ueb. d. Entwick. d. Seesterne u. Holothurien." Muller's Ardiir,
A. Krohn. "Beobacht. lib. Echinodermenlarven." Miiller's Archiv, 18(4.
('>'>'.)} II. Ludwig. "Ueb. d. primar. Steinkanal d. Crinoideen, nebst vergl. anat. Bemerk. ub. d. Echinodermen." Zeit.f. wiss. Zoo/., Vol. xxxiv. iSSo.
(">r,n) K. Metschnikoff. "Studien lib. d. Entwick. d. Echinodermen u. Nemertinen." Mem. .!< . J', : /i'rsfa>nr?. Scries VII., Tom. XIV., No. 8. 1869.
(501)' Joh. Miillcr. " Ueb. d. Larven u. d. Metamorphose d. EchinodcM men.' Alhandlnng,-n d. />>///'. Akad. (Five Memoirs), 1848, 49, 50. 52 (two Mnnoirs).
Joh. Miiller. " Allgemeincr Plan d. Entwicklung d. Echinodermen. Abhandl. d. Berlin. Akad., 1853.
1 The dates in this reference are the dates of publication.
(563). E. Selenka. "Zur Entwicklung d. Holothurien." Ztit. f. wiss. Zoo/., Ed. xxvn. 1876.
(564) E. Selenka. "Keimblatter u. Organanlage bei Echiniden." Zeit.f.wiss. Zool.t Vol. xxxni. 1879.
(565) Sir Wyville Thomson. " On the Embryology of the Echinodcrmata." Natural History Review, 1864.
(566) Sir Wyville Thomson. "On the Embryogeny of Antedon rosacetw." Phil. Trans. 1865.
(567) A. Agassiz. "Tornaria." Ann. Lyceum Nat. Hist. vin. New York, 1866.
(568) A. Agassiz. "The History of Balanoglossus and Tornaria." Mem. Amer. Acad. of Arts and Scien., Vol. IX. 1873.
(569) A. Gotte. " Entwicklungsgeschichte d. Comatula Mediterranea. " Archiv fur mikr. Anat., Bd. XII., 1876, p. 641.
(570) E. Metschnikoff. " Untersuchungen lib. d. Metamorphose, etc. (Tornaria)." Zeit.fiir wiss. Zool., Bd. XX. 1870.
(571) J. M tiller. " Ueb. d. Larven u. Metamor. d. Echinodermen." Berlin. Akad., 1849 and 1850.
(572) J. W. Spengel. "Bau u. Entwicklung von Balanoglossus." Tagebl.d. Naturf. Vers. Mtinchen, 1877.
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