Chapter XVIII: Crustacea185 (2)

Cumaceæ. The development of the Cumaceæ 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 antennæ, mandibles, and two pairs of maxillæ and the following seven pairs of appendages takes place very early. The pair of appendages behind the second maxillæ 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 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 maxillæ 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.

COPEPODA.

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[195], 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.

[195] The Pontellidæ form an exception to this statement, in that
they are provided with paired lateral eyes in addition to the
median one.

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 antennæ 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[196]. 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 1_) is uniramous, and usually formed of three joints which bear bristles on their under surface. The two posterior pairs of appendages are both biramous. The second pair of antennæ (_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 antennæ, 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 antennæ 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 antennæ and the mandibles: it 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.

[196] The term Nauplius was applied to the larva of Cyclops and
allied organisms by O. F. Müller under the impression that they
were adult forms.

[FIG. 229. SUCCESSIVE STAGES IN THE DEVELOPMENT OF CYCLOPS
TENUICORNIS. (Copied from Bronn; after Claus.)

A. B. and C. Nauplius stages. D. Youngest Copepod stage. In this
figure maxillæ and the two rami of the maxilliped are seen
immediately behind the mandible _md._
_oc._ eye; _at1._ first pair of antennæ; _at2._ second pair of
antennæ; _md._ mandible; _p1._ first pair of feet; _p2._ second
pair of feet; _p3._ third pair of feet; _u._ excretory
concretions in the intestine.]

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 maxillæ (fig. 229 B); at the same time the basal joint of the maxillæ develops a cutting blade. Three successive pairs of appendages (fig. 229 C) next become formed--the so-called maxillipeds (the homologues of the second pair of maxillæ), 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 cephalo-thoracic 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 antennæ, mandibles, maxillæ, the now double pair of maxillipeds (derived from the original single pair of appendages), and first pair of thoracic appendages (_p1_) are attached. The second pair of thoracic appendages (_p2_) is fixed to the first free segment, and the rudiment of a third pair (_p3_) projects from the second free segment. The first pair of antennæ 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 antennæ 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 maxillæ 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.

[FIG. 230. 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.

_at1._ first pair of antennæ; _at2._ second pair of antennæ; _md._
mandible; _mx._ maxillæ; _pm1._ outer pair of maxillipeds; _pm2._
inner pair of maxillipeds; _p1._ first pair of legs; _p2._ second
pair of legs; _z._ frontal organ; _i._ intestine; _o._ larval
eye; _b._ glandular body; _t._ organ of touch; _ov._ ovary; _f._
rod projecting from coalesced maxillipeds; _g._ cement gland;
_rs._ receptaculum seminis; _n._ nervous system; _te._ testis;
_v._ vas deferens.]

The development of Achtheres percarum, one of the Lernæopoda 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 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. antennæ (two pairs), mandibles, maxillæ, maxillipeds, and three pairs of swimming feet. The Nauplius appendages are greatly modified. The first pair of antennæ 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 maxillæ is small and palped. The maxillipeds (_pm1_ and _pm2_) are believed by Claus to be primitively a single biramous appendage, but early appear as two distinct structures[197], 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 (_p2_) 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.

[197] Van Beneden (No. 506) in the genera investigated by him
finds that the two maxillipeds are really distinct pairs of
appendages.

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 (_f_) projects, and attaches the larva to the mouth or gills of its host. The antennæ and jaws have nearly acquired their adult form. The nervous system consists of supra- and infra-oesophageal 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 maxillipeds of the male (fig. 230 E, _pm2_) 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, Lernæopoda, Brachiella and Hessia, _Ed. van Beneden_ (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 antennæ (two pairs), mandibles, maxillipeds, and the first pair of thoracic feet.

The first pair of antennæ 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[198]. The maxilla would, according to Claus, appear to be absent.

[198] 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
maxillæ detected by Claus in the adult.

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.

CIRRIPEDIA.

The larvæ 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 history of the four sub-orders, viz. Thoracica, Abdominalia, Apoda, and Rhizocephala.

Thoracica. The just hatched larvæ at once leave the egg lamellæ 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[199] which, though regarded by Claus as closely resembling the Copepod Nauplius (figs. 231 and 232 A), certainly has very marked peculiarities 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 _lh_), 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.

[199] 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.

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 (_lb_), 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 (_At1_) is uniramous, and the two posterior (_At2_ 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 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 larvæ 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 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.

[FIG. 231. NAUPLIUS LARVA OF LEPAS FASCICULARIS VIEWED FROM THE
SIDE.

_oc._ eye; _At. 1._ antenna of first pair; _At. 2._ antenna of
second pair; _md._ mandible; _lb._ labrum; _an._ anus; _me._
mesenteron; _d.sp._ dorsal spine; _c.sp._ caudal spine; _Vp._
ventral spine; _lh._ lateral horns.]

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 Archizoæa 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 Zoæa. The hind end of the shield is also produced into a long caudal spine (_c.sp_) 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 (_oc_) 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[200]. 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 (_Vp_) 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[201].

[200] 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.

[201] 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 Zoæa.

From the Nauplius condition the larvæ 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 maxillæ--and internal to these a pair of small prominences, which are perhaps equivalent to the second pair of maxillæ, 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 antennæ there may be seen just before the final moult the four-jointed antennæ of the Cypris stage with the rudiment of a disc on the second joint by which the larvæ 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 antennæ 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 antennæ are short, and the last of them is provided with olfactory hairs. The great upper lip and second pair of antennæ 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 maxillæ have become small papillæ 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 lamellæ, 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[202].

[202] 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
antennæ till a later period. He does not clearly describe its
opening, nor the organ which I have called the shell-gland.

[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; _t._ cement gland with duct to antenna.]

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 antennæ, and the cement gland (_t_) 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 antennæ 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 feet, and between the above-mentioned chitinous lamellæ, the cirriform feet are formed; and on their completion the natatory feet become thrown off and replaced by the permanent feet. In the Lepadidæ, in which the metamorphosis of the pupa stages has been most fully studied, the anterior part of the body with the antennæ 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 Lepadidæ 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 Lepadidæ "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 Balanidæ the embryonic valves are membranous and do not overlap, but do not present the peculiar fenestrated structure of the primordial valves of the Lepadidæ.

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 (_n_), 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 antennæ, a change in the position of the stomach, etc.

Abdominalia. In the Alcippidæ 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.

[FIG. 233. STAGES IN THE DEVELOPMENT OF THE RHIZOCEPHALA. (From
Huxley, after Fritz Müller.)

A. Nauplius of Sacculina purpurea.
B. Cypris stage of Lernæodiscus porcellanæ.
C. Adult of Peltogaster paguri.
_II._ _III._ _IV._ Two pairs of antennæ and mandibles; _cp._
carapace; _a._ anterior end of body; _b._ generative aperture;
_c._ root-like processes.]

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 antennæ, and a posterior prominence, the abdomen. In a later stage the abdominal prominence disappears, and the antennary processes, within which the true antennæ 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 antennæ 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 larvæ 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 anticipated 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 (1) in the large development of an oval dorsal shield (_cp_) 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.

OSTRACODA.

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 larvæ 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.

[FIG. 234. TWO STAGES IN THE DEVELOPMENT OF CYPRIS. (From Claus.)

A. Earliest (Nauplius) stage. B. Second stage.
_A´._ _A´´._ First and second pairs of antennæ; _Md._ mandibles;
_OL._ labrum; _Mx´._ first pair of maxillæ; _f´´_. first pair of
feet.]

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 however 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 antennæ is moreover very similar to the second and is used in progression. Neither of the pairs of antennæ 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.

[FIG. 235. STAGES IN THE DEVELOPMENT OF CYPRIS. (From Claus.)

A. Fourth stage. B. Fifth stage.
_Mx´._ first maxilla; _Mx´´._ and _f´._ second maxilla; _f´´._ first
pair of feet; _L._ liver.]

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 maxillæ and the first pair of feet; the second pair of maxillæ not being developed till later. The first pair appear as leaf-like curved plates (_Mx´_) more or less like Phyllopod appendages (Claus) though at this stage without an exopodite. The first pair of feet (_f´´_) 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 maxillæ acquire their pectinated gill plate (epipodite) and four blades; and in the fourth stage (fig. 235 A) the second pair of maxillæ (_Mx´´_) arises, as a pair of curved plates, similar to the first pair of maxillæ 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 antennæ becomes increased, and the posterior maxillæ develop a blade and become 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 (_f´´´_) and the maxillæ 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 permanent form; the second pair of maxillæ 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.

[FIG. 236. SIXTH STAGE IN THE DEVELOPMENT OF CYPRIS. (From Claus.)

_Mx´._ first maxilla; _Mx´´._ _f´._ second maxilla; _f´´._ and
_f´´´._ first and second pair of feet; _Fu._ caudal fork; _L._
liver; _S.D._ shell-gland.]

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 maxillæ and two following appendages) are very rudimentary.

The larvæ 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 Müller (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 Müller 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[203]. The more important of these are the following.

[203] For the characters of Nauplius _vide_ p. 460.

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 antennæ are biramous swimming feet with a hook used in mastication, and are innervated (?) from the suboesophageal 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 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 antennæ 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 palæontological and morphological. Claus indeed carries this view still further, and believes that the later Nauplius stages of the different Entomostracan groups and the Malacostraca (Penæus 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, Penæus 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 Protozoæa stage in which the maxillæ 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 Zoæa stage the chief features of which have already been fully characterised (_vide_ p. 465). Three more or less distinct types of Zoæa are distinguished by Claus. (_a_) That of Penæus, 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 Zoæa 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 many-chambered heart, two pairs of maxillipeds and the abdominal appendages in full activity.

4. A Mysis stage, which is only found in the macrurous Decapod larvæ.

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 Müller 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 Müller'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 Müller'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[204] 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.

[204] 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 Protozoæa
and earliest Cyclops stage. Yet if I understand him rightly, he
does not consider the Protozoæa 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.

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 Zoæa 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 Zoæa.

5. The presence of gill pouches (epipodites) on many of the appendages[205].

[205] Claus appears to consider it doubtful whether the
Malacostracan gills can be compared with the Phyllopod gill
pouches.

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 Müller commences his summary of the characters of the Zoæa in the following words[206]. "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 Zoææ, 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 Zoæa forms is secondary and not an ancestral Phyllopod peculiarity.

[206] _Facts for Darwin_, p. 49.

This is the main argument used by Claus against the Zoæa having any ancestral meaning. His view as to the meaning of the Zoæa may be gathered from the following passage. After assuming that none of the existing Zoæa types could have been adult animals, he says--"Much more probably the process of alteration of the metamorphosis, which the Malacostracan phylum underwent in the course of time and in conjunction with the divergence of the later Malacostracan groups, led secondarily to the three different Zoæa configurations to which probably later modifications were added, as for instance in the young form of the Cumaceæ. We might with the same justice conclude that adult Insects existed as caterpillars or pupæ as that the primitive form of the Malacostraca was a Protozoæa or Zoæa."

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 Zoæa 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 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 Zoæa stage in which the thoracic appendages were completely aborted. Claus maintains that the Zoæa 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 Zoæa 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 Protozoæa stage, but completely aborted in the Zoæa 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 Zoæa forms, its actual atrophy in the Penæus Zoæa, and its 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 Zoæa 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 larvæ of the Zoæa ancestors always developed the appendages in question. Such appendages might first only partially atrophy in a particular Zoæa 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 Zoæa, we should find in the larval history of this form that the limbs were developed in the pre-zoæal larval stages, partially atrophied in the Zoæa 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 Zoæa stage.