The Works of Francis Balfour 2-16

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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
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This historic 1885 book edited by Foster and Sedgwick is the second of Francis Balfour's collected works published in four editions. Francis (Frank) Maitland Balfour, known as F. M. Balfour, (November 10, 1851 - July 19, 1882) was a British biologist who co-authored embryology textbooks.

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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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

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Vol II. A Treatise on Comparative Embryology (1885)



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,

FIG. 166.

A. B. C.


(From Biitschli.)

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.