CHAPTER IV

THE METAMORPHOSES OF CRUSTACEA

The great majority of Crustacea are hatched from the egg in a form very different from that which they finally assume, and reach the adult state only after passing through a series of transformations quite as remarkable as those which a caterpillar undergoes in becoming a butterfly, or a tadpole in becoming a frog. Many of these young stages were known for a long time before their larval nature was suspected, and it is one of the curiosities of the history of zoology that, even after the actual changes from one form to another had been observed and described in several Crustacea, many eminent naturalists refused to believe in the possibility of their occurrence. This scepticism was largely due to the fact that the common fresh-water Crayfish, when hatched from the egg, has practically the same structure as the adult, and it was assumed that other Crustacea were developed in a similar fashion. Although certain cases of metamorphosis had been actually seen and described by naturalists in the eighteenth century, these observations were forgotten or misunderstood till they were confirmed by Mr. J. Vaughan Thompson, a naval surgeon stationed at Cork, the first part of whose "Zoological Researches" was published in 1828. Thompson's statements were much disputed at the time, but they have been confirmed by subsequent research, and it is now known that the majority of Crustacea undergo a more or less extensive metamorphosis after leaving the egg, although, as will be seen later, there are many important exceptions to this rule.

If a fine muslin net be towed at the surface of the sea on a calm day, and the contents turned out into a jar of sea-water, it will usually be found to have captured, among other things, clouds of animated specks, which dance in the water or dart hither and thither with great rapidity. Many of these specks, when examined with the microscope, will be found to be Crustacea. Besides adult animals belonging to various groups, such as the Copepoda, which pass the whole of their life swimming near the surface of the sea, there will be numerous larval stages of species which in their adult form live on the sea-bottom. The identification of the species to which the various larvæ belong is a matter of considerable difficulty, and, although the general course of development is now well known for all the chief groups of Crustacea, there are very many even of the common British species in which the larval transformations have not yet been worked out in detail.

As an example of the larval history of the higher Crustacea, we may take the case of the Common Shore Crab, _Carcinus mænas_ (Fig. 25). The young stages are common in tow-net gatherings round the British coasts in the summer-time. The youngest larvæ (Fig. 25, A) are translucent little creatures about one-twentieth of an inch long. They have the head and front part of the body covered by a helmet-shaped carapace, with a long spine standing out from the middle of the back, and another projecting, like a beak, in front.

The narrow abdomen or tail is very flexible, and can be doubled up under the body or stretched out behind; it ends in a forked telson. There are two pairs of swimming limbs, each with endopodite and exopodite, and the short antennules and antennæ are seen on either side of the rostrum. There are a pair of very large compound eyes, which are not set on movable stalks, but are under the front part of the carapace. The two-branched swimming feet are really the first and second maxillipeds (the mandibles, maxillulæ, and maxillæ, can be found in front of them), but none of the other thoracic limbs are yet developed, and, although the somites of the abdomen are distinct, there are no swimmerets. This type of larva is known as a _zoëa_, a name which was given to it when it was supposed to be an independent species of Crustacean. As a matter of fact, the zoëa just described is not quite the earliest stage of the Shore Crab, for when hatched from the egg it is without the spines on the carapace, and is slightly different in other respects. A few hours after hatching, however, it casts its skin for the first time, and becomes a fully-formed zoëa. It swims rapidly about at the surface of the sea, feeding on the minute floating animals and plants which are found there, and growing in size with repeated castings of its skin. In the later stages of the zoëa the rudiments of the hinder thoracic limbs and of the swimmerets appear as little buds. In the next stage (Fig. 25, B) all the appendages are present, the dorsal spine of the carapace has disappeared, the eyes are stalked and movable, and the animal has all the appearance of a little Crab, except that the abdomen is stretched out instead of being tucked up under the body, and the swimmerets are used as paddles in swimming. In this stage the larva, which is known as a _megalopa_, swims at the surface of the sea, but later it sinks to the bottom, and, moulting again, appears as a little Crab (Fig. 25, C), with tucked-up abdomen and swimmerets no longer adapted for locomotion.

Most of the true Crabs (Brachyura) have a larval history similar to that just described, and pass through zoëa and megalopa stages which differ only in details from those of _Carcinus_. The Anomura are also hatched as zoëæ, and one of the most remarkable forms common in tow-nettings in British waters is the zoëa of the little Porcelain Crabs (_Porcellana_--Fig. 26). In this larva the carapace has two long spines behind, and a rostral spine which is several times as long as the body of the animal. A great development of spines also characterizes the larva of _Munida_ (Fig. 27).

The larval form of the Common Lobster has already been described, and it will be noticed that the differences from the adult are much less than in the case of the Crab. From the fact that this larva has swimming exopodites on its legs, like the adult Mysidacea and Euphausiacea (formerly grouped together as "Schizopoda"), it is said to be in the "schizopod stage." The larva of the Norway Lobster (_Nephrops norvegicus_) is essentially of the same type, but the great development of the spines on the abdomen and of the forked telson gives it a striking appearance.

A very remarkable type of larva is found among the Spiny Lobsters and their allies (Scyllaridea). This larva, known by the name of _phyllosoma_ (Fig. 28), is very broad, thin, and leaf-like, and quite transparent, so that some of the larger kinds were formerly known as "Glass Crabs." The thin oval carapace does not cover the whole of the thoracic region, which is disc-shaped, with four pairs of long slender legs, each with an exopodite. The abdomen is relatively small. The intermediate stages between the phyllosoma and the adult are still very imperfectly known. In tropical seas phyllosoma larvæ of large size are found, sometimes reaching two or three inches in length. The larva of the Common Spiny Lobster (_Palinurus vulgaris_), however, does not exceed half an inch in length.

The Shrimps and Prawns of the tribe Caridea are mostly hatched as zoëæ, and pass through a "schizopod" stage comparable to that of the Lobster, in which they swim by means of exopodites on the legs. Some of the Prawns belonging to the tribe Penæidea, however, have a still more remarkable metamorphosis, which is very important on account of the resemblance of the earlier stages to those of the lower Crustacea. Fritz Müller discovered in 1863 that _Penæus_ is hatched from the egg as a _Nauplius_ (Fig. 29, A), a form of larva which was previously known among the Copepoda, Branchiopoda, and Cirripedes. The nauplius, unlike the larvæ which we have been considering, has an unsegmented body, and has only three pairs of limbs. The body is pear-shaped in outline, and near the front end is seen the median eye, sometimes called, from its presence in this type of larva, the "nauplius-eye"; the paired eyes are not yet developed. The three pairs of limbs are shown by their later development to be the antennules, antennæ, and mandibles; the first pair are unbranched, the second and third divided into exopodite and endopodite. It is interesting to notice that the antennæ and mandibles, which in the adult animal are so widely different that it is difficult to trace any resemblance between them, are in the nauplius almost identical in form. Further, the antennæ, instead of being placed in front of the mouth as in the adult, lie on either side of it, and each has at its base a hooked spine which projects inwards and serves for seizing particles of food and passing them into the mouth; the antennæ of the nauplius, in fact, serve as jaws, while it is only later that the mandibles take on this function.

In the further development of the larva, the body increases in length and becomes divided into somites which increase in number by new somites appearing behind those already marked off; the rudiments of the limbs also appear in regular order from before backwards; the dorsal shield of the nauplius grows out into a carapace, beneath which the paired eyes begin to develop in front. Thus after passing through _metanauplius_ and _protozoëa_ stages (Fig. 29, B) the larva becomes a _zoëa_ (Fig. 29, C), resembling that of the Crab already described in that the swimming organs are the maxillipeds, but differing in having the uropods well developed and forming a tail-fan at the end of the abdomen, the hinder thoracic somites marked off and their appendages present as rudiments, and the stalked eyes free from the carapace. This is followed by a _schizopod_ stage (Fig. 29, D), in which the prawn-like shape is assumed and the thoracic legs have large exopodites used for swimming. Later these exopodites diminish in size, though they do not quite disappear in the adult _Penæus_, and the function of swimming organs is taken over by the abdominal swimmerets.

In _Penæus_ the larvæ are of comparatively simple form, but in the allied genus _Sergestes_ the zoëa has a very remarkable appearance. The carapace is armed with long spines, each bearing two comb-like rows of secondary spines. The development of spines and other outgrowths of the surface of the body is a very common characteristic of organisms that, like these larvæ, float or swim in the open sea; its probable significance will be discussed in a later chapter.

The shrimp-like Euphausiacea have a larval development very like that of _Penæus_. Most, if not all, of the species are hatched from the egg in the nauplius stage, and pass through stages very similar to those described above. The adult animals, however, may be said to remain in the "schizopod" stage, since the exopodites of the thoracic legs remain large and are used in swimming.

Even among the Decapoda, however, there are many species that are hatched from the egg in a form that does not differ essentially from the adult, and are therefore said to have a direct development. This is often the case with species which live in fresh water or in the depths of the sea. For example, the young of the fresh-water Crayfish (Fig. 30), when hatched, possess all the appendages of the adult except the first pair of swimmerets and the uropods, or outer plates of the tail-fan. The carapace is almost globular, owing to the presence inside the body of a large amount of food-yolk, which supplies the nourishment necessary for the young animal in the early stages of its development. The chelæ have hooked tips, by means of which the young animal clings securely to the swimmerets of the mother. After a time it moults, and the uropods are set free, the chelæ lose their hooked tips, the carapace assumes nearly its final shape (the food-yolk having been largely absorbed), and the young Crayfish leaves the protection of its parent, to shift for itself. The essential point of difference between the development of the Crayfish and that of the closely related Lobster (see Fig. 8, p. 28) is not so much that the changes in structure which occur after hatching are less profound in the former case, but that there is no free larval stage. In the Lobster the earlier stages are capable of independent existence, and they differ from the full-grown animal not only in structure, but also in habits, swimming at the surface instead of creeping at the bottom of the sea.

A similar case to that of the Crayfishes is found in the River Crabs of tropical countries, belonging to the family Potamonidæ. These Crabs are as closely related to some marine Crabs as are the Crayfishes to the Lobsters, yet the difference in their mode of development is even more pronounced. Instead of beginning life as minute pelagic zoëæ, they leave the shelter of the mother's abdomen as perfectly-formed little Crabs (Fig. 31).

Amongst the Decapoda, instances of direct development like those just described are exceptional, but in some of the other orders of the Malacostraca direct development is the rule. In the great division Peracarida, as we have already seen, the females are provided with a pouch, or marsupium (from which the name of the division is derived), in which the eggs are carried. Within this pouch the young undergo the whole of their development, and they only leave it, as a rule, when they have attained the structure of the adults. Among the more familiar representatives of this division, the Sand-hoppers (Amphipoda), the Woodlice (Isopoda), and the Opossum Shrimps (Mysidacea), may be mentioned as examples of this mode of development. The Woodlice and their immediate allies differ a little from the other members of the division in the fact that the young leave the brood-pouch with the last pair of legs still undeveloped, though in other respects they are like miniature adults.

In those Crustacea which have a direct development without free-swimming larval stages, it is sometimes possible to find traces of such stages in the early development of the embryo. This is shown most clearly, perhaps, in the Opossum Shrimps (Mysidacea). In these the embryo becomes free from the egg-membrane (or may, in a sense, be said to "hatch") at a very early stage, and lies free within the brood-pouch as a maggot-shaped body, on which three pairs of rudimentary limbs can be made out. The later development shows that these three rudiments correspond to the antennules, antennæ, and mandibles, so that the maggot-shaped embryo is, in fact, a disguised nauplius without the power of swimming or of leading an independent existence. In other cases--as, for instance, in the Crayfish, where the earlier stages are confined within the egg-membrane (or "egg-shell")--the nauplius stage, although more difficult to examine, is quite as well marked.

Of the other groups of the Malacostraca, the Syncarida and Leptostraca are hatched in nearly the adult form, but the Stomatopoda have a long series of larval stages. These larvæ (Fig. 32) are all distinguished by the large size of the carapace, which in some cases envelops the greater part of the body. Some Stomatopod larvæ, in the warmer seas, attain to a relatively great size, sometimes exceeding 2 inches in length, and their glass-like transparency gives them a very striking appearance.

As we have seen, it is exceptional to find a free-swimming nauplius larva among the Malacostraca, but it is the commonest larval stage in the other subclasses of Crustacea. Most of the Branchiopoda are hatched in this form (Fig. 33), and reach the adult state by a very gradual series of changes in which new somites and appendages are added in regular order from before backwards till the full number is reached. The Water-fleas (Cladocera), however, differ from most of the other Branchiopoda in having a direct development. The eggs are carried in a brood-pouch under the back of the carapace, and in this the embryos undergo their development. In the common _Daphnia_, for instance, numerous eggs or young can generally be seen through the transparent carapace (see Fig. 12, p. 37).

Many of the Ostracoda have a direct development, but in some cases the young animal, on hatching, has only the first three pairs of appendages, and is therefore regarded as a nauplius, although it possesses a bivalved shell like that of the adult, and is very unlike the nauplius larvæ of other Crustacea.

Most of the Copepoda also leave the egg in the nauplius stage; and, indeed, it was to the young of the common fresh-water _Cyclops_ (Fig. 34) that the name of _Nauplius_ was first given by the Danish naturalist, O. F. Müller, in the eighteenth century, in the belief that it was an adult and independent species of Crustacea. In the Copepoda, the changes which transform the nauplius into the adult are gradual, and consist chiefly in the successive addition of new somites and appendages.

The development of the Cirripedia is of special interest, since it was the discovery of the larval stages by J. Vaughan Thompson that first demonstrated to naturalists that the Barnacles were Crustacea and not, as had been supposed, Molluscs. The earliest stage is generally a nauplius (Fig. 35, A) of very peculiar and characteristic form, with a pair of horns projecting sideways from the front corners of the dorsal shield, and a forked spine on the under-side behind. The later development is very unlike those which have been described above, for after a series of nauplius stages the larva passes suddenly, at a single moult, into a stage in which the body and limbs are enclosed in a bivalved shell (Fig. 35, B). From the superficial resemblance of the shell to that of an Ostracod, this is known as the _cypris_ stage. Through the valves of the shell a pair of large compound eyes can be seen, as well as six pairs of two-branched swimming feet, while in front a pair of antennules project between the valves. On each antennule is a sucker-like disc by means of which the larva, after swimming freely for some time, attaches itself to a stone or some other object, where it remains fixed for the rest of its life. A cementing substance produced by a gland at the base of the antennules attaches the front part of the head firmly to the support; the valves of the shell are cast off, and replaced by the rudimentary valves of the adult shell; the six pairs of swimming feet grow out into tendril-like cirri; the compound eyes disappear, and the animal assumes the structure of the adult.

The parasitic Rhizocephala have a very remarkable life-history, which will be described in a later chapter; but it may be mentioned here that their free-swimming larval stages resemble very closely those of the ordinary Barnacles. It was the discovery of this fact which led to its being recognized that the Rhizocephala are highly modified and degenerate Cirripedes, although their structure in the adult state gives little evidence of their affinities.

A number of interesting problems in speculative biology are suggested by the larval stages of Crustacea. A full discussion of these problems would involve matters too technical for these pages, but some indication of the broader issues may be attempted.

The obvious question, Why do some Crustacea pass through a complicated metamorphosis while others do not? is, like many obvious and simple questions, one of the most difficult to answer. It will be pointed out later, in dealing with the fresh-water Crustacea, that one of the most general characters of fresh-water animals as compared with their marine allies is the absence of free-swimming larval stages. This applies, for instance, to the case of the Crayfishes and the marine Lobsters, and to that of the River Crabs, as compared with those which live in the sea. But it does not apply to all fresh-water Crustacea, and, on the other hand, there are many cases of direct development in marine species.

Some of the advantages gained by the possession of free-swimming larval stages are obvious enough. Many Crustacea which live on the sea-bottom, and are not very powerful swimmers, have their progeny scattered far and wide by winds and currents while in the surface-living larval stages. In the extreme case of the Barnacles, which are fixed to one spot when adult, a locomotive larval stage is clearly a necessity. But, here as elsewhere, to demonstrate the usefulness of any character is to go only a very little way towards explaining its origin. Moreover, the mere necessity for a locomotive larva throws no light on the remarkable resemblances between the larval stages of widely different species. In the adult state, a Branchiopod, a Copepod, an Ostracod, a Barnacle, and a Penæid Prawn, are separated by enormous differences of form and structure; yet, as we have seen, all these are hatched from the egg as six-limbed nauplius larvæ differing from each other only in trivial details. It seems hardly possible to imagine any other interpretation of this very striking fact than is afforded by the theory of Evolution. We are forced to assume that all these diverse forms of Crustacea are descended from very similar or identical ancestral types, and that the modifications arising in the course of their evolution have affected the adult but not the larval stages. Some naturalists would go farther than this, and would apply the so-called "theory of recapitulation" to the larval stages of the Crustacea. According to this theory, the stages in the development of any animal tend to recapitulate, more or less closely, the history of the race. Thus it is assumed, for instance, that the nauplius reproduces the structure of a six-limbed ancestral form, from which, in the distant past, all the diverse branches of the Crustacean class took their origin. There are, however, considerable difficulties in the way of this view. That some such ancestral type did exist may be regarded as tolerably certain; that it resembled in its adult state the nauplius larvæ of present-day Crustacea is, on the whole, unlikely; but it is not at all improbable, whatever its adult structure may have been, that it hatched from the egg as a nauplius larva.

With regard to some of the other larval forms, it is possible to speak with a little more confidence. There are good grounds for believing, apart from the evidence of development, that the Lobster and its allies have descended from Crustacea which, like the existing Euphausiacea, possessed swimming branches (exopodites) on the thoracic legs; and there seems no reason to doubt that the "schizopod" larva of the Lobster does recapitulate this stage in the evolution of the race. On the other hand, it is impossible to believe that any of the ancestors of the Shore Crab resembled, even remotely, the zoëa stage with which the life-history of the individual now begins.