The Works of Francis Balfour 2-18
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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 XVIII CRUSTACEA
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.
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.
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 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 PHYLLOPOD 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.
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