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 larvae 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.
[Illustration: FIG. 25--LARVAL STAGES OF THE COMMON SHORE CRAB
(_Carcinus maenas_--SEE PLATE IX.). (Partly after Williamson.)
A, Young zoea, shortly after hatching; B, megalopa stage; C, young Crab.
A x 20, B and C x 10]
As an example of the larval history of the higher Crustacea, we may take
the case of the Common Shore Crab, _Carcinus maenas_ (Fig. 25). The young
stages are common in tow-net gatherings round the British coasts in the
summer-time. The youngest larvae (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 antennae 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, maxillulae, and maxillae, 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 _zoea_, a name which was given to it when it
was supposed to be an independent species of Crustacean. As a matter of
fact, the zoea 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 zoea. 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 zoea 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.
[Illustration: FIG. 26--LAST LARVAL STAGE OF THE COMMON PORCELAIN CRAB
(_Porcellana longicornis_--SEE FIG. 41, p. 113). x 9. (After Sars.)]
Most of the true Crabs (Brachyura) have a larval history similar to that
just described, and pass through zoea and megalopa stages which differ
only in details from those of _Carcinus_. The Anomura are also hatched
as zoeae, and one of the most remarkable forms common in tow-nettings in
British waters is the zoea 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).
[Illustration: FIG. 27--FIRST LARVAL STAGE OF _Munida rugosa_ (SEE PLATE
VI.). x 10. (After Sars.)]
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 larvae 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.
[Illustration: FIG. 28--THE PHYLLOSOMA LARVA OF THE COMMON SPINY LOBSTER
(_Palinurus vulgaris_--SEE PLATE V.). MUCH ENLARGED. (After J. T.
Cunningham.)]
The Shrimps and Prawns of the tribe Caridea are mostly hatched as zoeae,
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 Penaeidea, 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
Mueller discovered in 1863 that _Penaeus_ 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 larvae 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, antennae, and mandibles; the first pair
are unbranched, the second and third divided into exopodite and
endopodite. It is interesting to notice that the antennae 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 antennae, 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 antennae
of the nauplius, in fact, serve as jaws, while it is only later that the
mandibles take on this function.
[Illustration: FIG. 29--LARVAL STAGES OF THE PRAWN--_Penaeus_ (SEE PLATE
IV.). x 45. (After F. Mueller.)
A, Nauplius; B, young zoea; C, older zoea; D, early "schizopod" stage]
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
_protozoea_ stages (Fig. 29, B) the larva becomes a _zoea_ (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 _Penaeus_, and the function of swimming organs is taken over by
the abdominal swimmerets.
In _Penaeus_ the larvae are of comparatively simple form, but in the
allied genus _Sergestes_ the zoea 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 larvae, 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
_Penaeus_. 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.
[Illustration: FIG. 30--NEWLY-HATCHED YOUNG OF A CRAYFISH (_Astacus
fluviatilis_). ENLARGED]
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 chelae 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 chelae 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 Potamonidae. 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 zoeae, they leave
the shelter of the mother's abdomen as perfectly-formed little Crabs
(Fig. 31).
[Illustration: FIG. 31--YOUNG SPECIMEN OF AN AFRICAN RIVER CRAB
(_Potamon johnstoni_), TAKEN FROM THE ABDOMEN OF THE MOTHER. MUCH
ENLARGED
The adult of an allied species is figured on Plate XXIII]
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, antennae, 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 larvae (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 larvae, 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.
[Illustration: FIG. 32--EARLY LARVAL STAGE OF A SPECIES OF SQUILLA,
PROBABLY _S. dubia_. x 10. (After Brooks.)]
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).
[Illustration: FIG. 33--LARVAL STAGES OF THE BRINE SHRIMP (_Artemia
salina_). (After Sars.)
A, Nauplius, just hatched; B-E, later stages, showing progressive
increase in number of somites and appendages. The adult form of this
species is shown in Fig. 55, p. 164]
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 larvae of other Crustacea.
[Illustration: FIG. 34--EARLY NAUPLIUS LARVA OF A COPEPOD (_Cyclops_).
MUCH ENLARGED. (From Lankester's "Treatise on Zoology.")
_a'_, Antennule; _a''_, antenna; _gn_, jaw-spine of antenna; _lbr_,
upper lip; _md_, mandible]
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. Mueller, 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.
[Illustration: FIG. 35--LARVAL STAGES OF THE COMMON ROCK BARNACLE
(_Balanus balanoides_--SEE PLATE III.)
A, Nauplius stage (after Hoek); B, cypris stage (after Spence Bate)]
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 Penaeid 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 larvae 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 larvae 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 zoea stage with which the life-history of
the individual now begins.