and, indeed, our knowledge of this whole case of Symbiosis, to the
beautiful observations of Eisig. Starting from the hypothesis that the
mutual relations could only be the outcome of natural selection, Eisig
pointed out that this partnership must offer some advantage not to one
partner only, but to both; otherwise it could not have arisen through
selection. The advantage to the sea-anemone is obvious enough; since of
itself it can only move very slowly, and is usually firmly fixed in one
place, it is easy to see that it would be useful to it to be carried
about on the floor of the sea by the hermit-crab, and to get its share
of the hermit-crab's food. But the service yielded to the hermit-crab
by the sea-anemone in return is not nearly so apparent. Eisig made
an observation in the Zoological Station at Naples which solved this
riddle. He saw an octopus attack the hermit-crab and attempt to draw
it out of its shell with the point of one of its eight arms. But before
this had succeeded there sprang from the body of the sea-anemone a
large number of thin worm-like threads which spread over the arm of
the robber, who immediately let go his hold of the crustacean and
troubled himself no further with it. These threads, called acontia,
are thickly beset with stinging-cells, which must at least cause a
violent smarting on the soft skin of the octopus. Thus we see that the
Actinia instinctively defends its partner from attacks, and does it so
effectively that we need not wonder how the instinct to provide itself
with Actiniæ could have arisen in the hermit-crab. But the acontia seem
to have been greatly strengthened in the course of the sea-anemone's
association with hermit-crabs, for they do not occur in all forms, and
they are most highly developed in those which live in Symbiosis with
crustaceans.
[Illustration: FIG. 34. Hermit-crab (_E_), within a Gasteropod shell,
on which a colony of _Podocoryne carnea_ has established itself.
From the common root-work (which is not clearly shown) there arise
numerous nutritive polyps with tentacles (_np_), among which are
smaller 'blastostyle' polyps with a circle of medusoid buds (_mk_),
spine-like personæ (_stp_), and on the margin of the mollusc shell a
row of defensive individuals (_wp_). _F_, antennæ. _Au_, eyes of the
hermit-crab; slightly enlarged.]
In this case the structural change, the transformation of the
mesenteric filaments that occur in all Actiniæ into projectile
acontia, is comparatively slight, but in another partnership between
hermit-crabs and polyps the latter have undergone a much more marked
adaptation. At Naples _Eupagurus prideauxii_ is one of the commonest
hermit-crabs. It lives at a depth of about a hundred feet, and is
often brought to the Zoological Station by the fishermen in large
quantities. Its borrowed mollusc shell often bears a little polyp,
_Podocoryne carnea_ (Fig. 34), which forms colonies of often several
hundred individuals, arising from a common root-work of stolons which
covers the shell. The polyp colony is composed of different kinds
of individuals or personæ, illustrating the principle of division
of labour: it includes (1) nutritive persons (_np_) which possess a
proboscis, mouth, and tentacles on their club-shaped bodies; (2) much
smaller blastostyles (_bl_), that is to say, polyps with degenerate
mouth and tentacles, which are wholly given over to the production
of buds (_mk_), which then develop into sexual animals, little
free-swimming medusoids; and (3) protective personæ in the form of hard
spines (_stp_), beneath the shelter of which the soft polyps withdraw
when the mollusc shell is rocked about on the sea-floor by the rolling
of the waves. In addition to these three different kinds of individuals
or personæ there are also (4) defensive polyps (_wp_) of long,
thread-like shape, thickly set with stinging-cells, but possessing
neither mouth nor tentacles. It might at first be thought that these
are for the defence of the colony, but this is not so; the fact is
that they rather serve for the direct defence of the hermit-crab.
This is indicated by the position they occupy in the colony; they are
not regularly distributed over the surface, but are ranged round the
edge, and, indeed, only on the edge which surrounds the opening of
the mollusc shell. Here these defensive polyps stand in close array,
sometimes spirally contracted, sometimes hanging loosely down over
the hermit-crab like a fringe. Their function, like the acontia of
Actiniæ, is to defend the crab when an enemy tries to follow it within
the shelter of its domicile. This can easily be demonstrated by drawing
out the hermit-crab from the Gasteropod shell, and, when the colony has
settled down again, seizing the shell with the forceps and drawing it
slowly through the water. The water-stream which then flows upon the
shell mimics the attack of an enemy, and immediately all the defensive
polyps, as at a given signal, strike from above downwards, and repeat
this three or four times; they are scaring off the supposed enemy.
In this species of polyp a special form of individual has developed
with a quite definite position in the colony, and furnished with a
special instinct or reflex mechanism which is directly useful only to
the crab, and has therefore, in a sense, arisen for its advantage. This
can quite well be explained through natural selection, for indirectly
these polyps are also of use to the colony, inasmuch as they protect
their valuable partner, and thus render it possible for the hydroid
colony to make the partnership of use to the hermit-crab as well as to
itself.
This mutual arrangement thus satisfies the requirement which, from
the selectionist point of view, must be made in regard to all that is
new--that it must be useful to its possessor.
If it be asked what service the hermit-crab renders to the polyp colony
in return, the answer is that, as in the symbiosis with sea-anemones,
the hermit-crab carries the polyps to their food, which is also its
own. Hermit-crabs eat all sorts of animal food, living or dead, which
they find on the sea-floor, and the remains of their meal fall to
the share of the polyps. Once, without special intention, I laid a
hermit-crab with its polyp colony in a flat vessel of sea-water beside
a bright green living sponge. After some time the majority of the
polyps had become bright green; they had filled themselves with the
green cells of the sponge.
I do not know how else we should picture to ourselves the origin
of symbiotic instincts in such lowly animals except through the
transmission and augmentation of variations in the instincts of the
two partners--variations which made their possessors more capable of
survival. Mollusc shells, ever since there were any, must have served
as a foundation and point of attachment for polyp colonies; as a
matter of fact, we find to-day on mollusc shells many kinds of polyp
colonies which show no special adaptation to a life of partnership
with hermit-crabs. From such indifferent associations a symbiotic
one must gradually have been evolved in some instances, through the
preservation and augmentation of every useful variation, both of
instincts and reflex actions, as well as of form and structure. I
shall not attempt to trace the course of this evolution in detail, but
it is obvious that the development of defensive polyps, and of their
instinct to defend the crustacean, can be interpreted neither as due
to any direct influence nor as due to the effect of use, but only to
the utility of this arrangement, the beginnings of which--polyps with
stinging-cells--were already present. Their augmentation and perfecting
must be referred entirely to natural selection. It is the same with
adaptations which do not refer directly to the crustacean partner,
but rather to the disposition of the polyps on the shell. The spinous
personæ which protect the softer polyps from being crushed by being
rolled about on the pebbles by the waves cannot possibly be regarded
as the direct result of this crushing. But it is obvious that some
such colonies must have had among their members some with a stronger
external skeleton, and therefore less easily crushed than the rest, and
this would lead to their more frequent survival.
No adaptation seems to have taken place in the hermit-crab in this
case, but that is probably only apparently the case; the probability
is that it would not tolerate the presence of the polyp-colony on the
shell unless its instinct compelled it thereto, just as its instinct
impels it to cover itself with sea-anemones, and fearlessly to grasp
the dangerous animal, which, however, only shows its partner its softer
side. Truly, such transformations of instinct are wonderful enough, but
that they should have come about through intelligence is here quite
inconceivable; there remains nothing but natural selection.
A case in which no apparent corporeal adaptations have occurred, but
which depends altogether on slight modifications of the instincts, is
afforded by the well-known relations between ants and aphides. These
two groups of insects live in a kind of symbiosis, although they are
by no means inseparably connected with each other. Wherever strong
colonies of aphides cover the young shoots of a plant, such as a
stinging-nettle, a rose, or an elder, we almost always find ants which
walk cautiously about among the plant-lice, often in great numbers,
stopping now and again to stroke them with their antennæ, and then
licking up the sweet juice from the intestine which they now give
forth. Darwin showed by experiment that the aphides retain this juice
if no ants are on the spot, and only give it off when ants are put
beside them. Herein lies the proof that we have again to do with a
case of modification of instincts. This juice is, of course, not the
secretion of special glands, as it was still believed to be in Darwin's
time, and it does not come from the so-called 'honey-tubes' situated on
the back of the abdomen of the aphides; it is simply their excrement,
which is liquid like their food, and the voiding of it has become
instinctively connected with the presence of the friendly ants.
That the aphides are not in any way afraid of the ants implies, in
itself, a modification of their instinct, for these poisonous insects,
prone to biting, are otherwise much dreaded in the insect world.
Moreover, the aphides, harmless as they seem, are not quite without
means of defence, although these are never used against the ants.
Other animals which approach them they bespatter with the sticky,
oily secretion prepared in the so-called 'honey-tubes' already noted,
squirting it especially into the eyes of an assailant, so that the
attack is abandoned.
Of course the aphides have no idea wherein the utility of their
friendship for the ants consists, but it is not difficult for us to
discover it, since the ants, by their mere presence in the aphid
colony, frighten and keep off their enemies. We see, then, that the
conditions for a process of natural selection are here afforded:
the instinct to be friendly to the ants is thoroughly useful, and
the instinct of the ants to seek out the aphides, and, instead of
devouring them, to 'milk' them, is also advantageous; it must be an
old acquisition, an instinct early developed, for in several species it
has gone so far that the aphides are carried into the ants' nest, and
are there (as one might say) kept and tended as domesticated animals.
A pretty case of symbiosis between two animals is reported by
Sluiter, and I mention it because it concerns a vertebrate animal,
and intelligence has something to do with it. In the neighbourhood
of Batavia there are frequently to be found on the coral reefs
large yellow sea-anemones, with very numerous and comparatively
long tentacles, and a little brightly-coloured fish, of the genus
_Trachichthys_, makes use of these forests, beset with stinging-cells,
to find security from its enemies. These appear to be numerous, for
in an aquarium, at any rate, the little fish very soon falls a victim
to one or other of them, unless he is supplied with the protective
sea-anemones. When this is the case it swims blithely about among the
tentacles, and the sea-anemone does not sting it; for there has been a
modification of instinct on its part as well as on that of the fish.
The advantage it gains from the fish is, that the latter brings large
morsels of food--in the aquarium, pieces of meat--into the anemone's
mouth. In doing so it tears away fibres for itself, and even if the
Actinia has swallowed pieces too quickly, the fish pulls them half out
of the gullet again, and only relinquishes them to be consumed by its
partner when it has satisfied its own appetite. In this case, again,
the modification of the instinct is the only adaptation which has been
brought about by the symbiosis, and its origin seems difficult to
understand. How can the fish have first formed the habit of putting
its prey into the mouth of the anemone instead of eating it directly?
Although in many cases it is difficult to guess at the beginnings of
a process of selection, because they are scarcely discoverable in
the subsequently accumulated variations, yet in this instance we may
perhaps picture them to ourselves in this way: The fish was in the
habit of letting fall pieces of food which could not be swallowed
whole, and of diving down upon them repeatedly, to tear off a fragment
each time. As the sea-floor in flat places is often covered with
sea-anemones, these pieces would often sink down upon one, which would
welcome it as a dainty, and set about swallowing it, slowly in its own
fashion. The fish must then have found by experience that it could tear
off little bits much more easily from a piece that was held firmly by
the anemone than from one that was lying loose upon the ground, and
this may have caused it to do intentionally what was at first done by
chance. But the sea-anemone, suffering no harm from the fish--indeed,
its association of ideas, if I may use the expression, must rather
have been little fishes and unexpected food--had no cause to shoot
its microscopic arrows at it, and did not do so even when the fish
concealed itself among the tentacles. This latter habit on the part of
the fish would be developed into an instinct through natural selection,
since the individuals that most frequently exhibited it would be the
best protected, and therefore, on an average, the most likely to
survive. Whether the benevolent attitude of the anemone towards the
fish is to be regarded as the expression of an instinct is open to
dispute, for it is quite conceivable that each individual sea-anemone
is disposed to gentleness by the behaviour of the fish, and so the
development of a special hereditary instinct was unnecessary, because
without it each anemone reacted in the manner most likely to secure its
own advantage[7].
[7] Since the above was written Plate has observed several similar
cases in the Red Sea. A little fish lives along with the anemone,
_Crambactis aurantiaca_, a foot in size, and not only conceals itself
among its tentacles, but remains among them when the anemone draws them
in. These fishes, therefore, must be immune against the stinging-cells
of the sea-anemone; and in the same way another species of fish
appears to be immune from the strong poison secreted by sea-urchins
of the genus _Diadema_ from the points of their spines, among which
the fishes live. This relation certainly seems more like a one-sided
adaptation on the part of the fishes than a true symbiosis, but in the
cases observed by Sluiter the return service of the fishes seems to
be regularly rendered. Here, as everywhere else in nature, there are
transition stages, and a one-sided protective relation may gradually,
under favourable circumstances, be transformed into a symbiosis.
The same may be true of the fish as far as laying its booty in the
mouth of the anemone is concerned; there may be no inherited instinct
in this; it may be an intelligent action, which is learnt anew in the
lifetime of each individual.
It might of course be objected to this interpretation that the
beginning of the process, namely, the assumption that chance fragments
from the food of the fish falling just on the anemone is very
improbable; but I once observed that flat rocks washed over by the
sea on the Mediterranean coast (not far from Ajaccio) were so thickly
covered with green anemones that at first I took the green growth for
some strange sea-grass new to me until I had pulled up a little tuft
of the supposed plants and identified them as the soft tentacles of
_Anthea cereus_. Anemones must be equally abundant in the tropical seas
of Java, and a sinking fragment must often alight on the mouth of one
of them.
Much attention and keen discussion have in the last few decades been
focussed on cases of symbiosis between unicellular Algæ and simple
animals. A good example is our green fresh-water polyp, _Hydra viridis_
(Fig. 35, _A_). Its beautiful colour is due to chlorophyll, and it was
long a matter of surprise that animals should produce chlorophyll,
which is a characteristic and fundamental important substance of
assimilating plants, until Geza Entz and M. Braun demonstrated that the
green did not belong to the animal at all, but to unicellular green
Algæ, so-called Zoochlorellæ, which are embedded in the endoderm cells
of the polyps in great numbers (Fig. 35, _zchl_). As these algoid
cells assimilate, and thus liberate oxygen, their presence is of
advantage to the polyp. That--as was at first believed--they also yield
nourishment to the polyp I consider very probable, notwithstanding
the apparently opposed results of the experiments of so acute an
observer as von Graff, for I have seen a large number of these animals
thrive for months, and multiply rapidly by budding in pure water which
contained no food of any kind. In favour of this view, too, are some
observations, to be cited presently, on unicellular animals, in regard
to whose nourishment by the zoochlorellæ living within them there can
be no doubt at all.
[Illustration: FIG. 35. _Hydra viridis_, the Green Fresh-water Polyp.
_A_, the entire animal, greatly enlarged. _M_, the mouth. _t_,
tentacles. _sp_, testis. _ov_, ovary, both in the ectoderm. _Ei_, a
ripe ovum, already green, in process of being extruded. After Leuckart
and Nitsche.
_B_, section of the body-wall, about the position of the ovary in _A_.
_Eiz_, the ovum lying in the ectoderm (_ect_), in which zoochlorellæ
(_zchl_), belonging to the endoderm (_ent_), have already migrated
through the supporting middle lamella (_st_). _eik_, nucleus of ovum.
After Hamann.]
The little algæ on their part find a peaceful and relatively secure
abode within the polyp, and they apparently do not occur outside of
it, at least they do not now migrate from outside into the animal,
but are carried over as a heritable possession of the polyps from
one generation to another, and in a very interesting manner, namely,
by means of the eggs, and by these alone. As Hamann has shown, the
zoochlorellæ migrate at the time when an egg is formed in the outer
layer of the body of the polyp (Fig. 35) from the inner layer outwards,
piercing through the supporting layer between them (st) and penetrating
into the egg (_B_, _Eiz_). They make their way only into the egg, not
into the sperm-cells, which in any case are too small to include them.
Thus they are absent from no young polyp of this species, and it is
easy to understand why earlier experimental attempts to rear colourless
polyps from eggs could never succeed even in the purest water.
[Illustration: FIG. 36. _A_, _Amœba viridis_. _k_, the nucleus.
_cv_, contractile vacuole. _zchl_, the zoochlorellæ. _B_, a single
zoochlorella under high power. After A. Gruber.]
Quite similar green algæ live in symbiosis with unicellular animals,
as, for instance, with an amœba (Fig. 36) and with an Infusorian of the
genus _Bursaria_. In the Zoological Institute in Freiburg there is a
living colony of a green amœba and a green _Bursaria_, both of which
came from America, sent to us some years ago by Professor Wilder, of
Chicago, inside a letter with dried _Sphagnum_, or bog-moss. The plants
came from stagnant water in the Connecticut valley in Massachusetts.
That in this case the zoochlorellæ are of use to the animals within
which they live, not only by giving off oxygen, but also by yielding
food-stuff, has been proved by A. Gruber, who bred the two green
species for seven years in pure water which contained no trace of any
kind of organic food for them. Nevertheless, they multiplied rapidly,
and still form a green scum on the walls of the glass in which they are
kept. They only die away when they are kept in the dark, where the algæ
are unable to assimilate; then one green cell after another wanes and
disappears, and, in consequence, their hosts also die from the double
cause of lack of oxygen and lack of food.
Even in this case the symbiotically united organisms have not remained
unaltered. The algæ at least differ from others of their kind in their
power of resistance to living animal protoplasm. They are not digested
by it, and we may infer from this that they possess some sort of
protective adaptation against the dissolving power of animal digestive
juices; they must, therefore, have undergone some variation, and
adapted themselves to the new situation. Probably their cell-membrane
has become impenetrable to the stuffs which would naturally digest
them, an adaptation which could not be referred to direct effect or to
use, but only to the accumulation of useful variations which cropped
up--in other words, to natural selection. That any adaptive variation
has taken place on the part of the host, whether polyp, amœba, or
Infusorian, cannot be made out. None of these have altered their
original mode of life; they do not depend on the nourishment afforded
by the algæ, but feed on other animals, if these come in their way,
and they live in water rich in oxygen like other species allied to
them, and therefore are not altogether dependent on the algæ in this
connexion; but they can no more help having their partners than the pig
can help having Trichinæ in its muscles.
Similar plant-cells, not green however, but yellow, called
zooxanthellæ, live in great numbers in the endoderm of various
sea-anemones and in the soft plasmic substance of many Radiolarians.
In both these cases we must look for the benefit they confer on their
host in the oxygen they give off, for, like the green zoochlorellæ,
they break up carbonic acid gas in the light, and give off oxygen;
they no longer occur, as far as is known, in a free state, but are
always associated with the host, and they must therefore have altered
in constitution, and have adapted themselves to the conditions of the
symbiosis.
Higher plants, too, sometimes have symbiotic relations with animals;
the most remarkable and best-known example is the relation between ants
and certain trees, in which the ants protect trees which afford them in
return both a dwelling-place and food. We owe our knowledge of these
cases to Thomas Belt and Fritz Müller, and more recently it has been
materially increased by Schimper's researches.
In the forests of South America there grow 'Imbauba,' or
candelabra-trees, species of the genus _Cecropia_, which well deserve
their name, for their bare branches stretch out like candelabra,
and bear little bunches of leaves only at their tips. These leaves
are menaced by the leaf-cutting ants of the genus _Œcodoma_, which
attack numerous species of plants in these regions, often in tens of
thousands, biting off the leaves, cutting them in pieces on the ground,
and carrying them on their backs piece by piece to their nests. There
they use them to make a kind of compost heap, on which fungi, to which
the ants are very partial, readily grow. The candelabra-tree protects
itself from these dangerous robbers, inasmuch as it has established an
association with another ant (_Azteca instabilis_), which finds a safe
dwelling-place in its hollow, chambered stem (Fig. 37, _A_), and feeds
on a brown sap which oozes from the inside. On the stem there are even
little pits regularly arranged in definite places (_E_), through which
the female of _Azteca_ can easily bore her way into the interior. There
she lays her eggs, and soon the whole interior of the trunk teems with
ants, which come trooping out whenever the tree is shaken.
[Illustration: FIG. 37. _A_, a piece of a twig of an Imbauba-tree
(_Cecropia adenopus_), with the leaves cut off. At the leaf-bases
are the hair-cushions (_P_). _E_, the opening for the associated ant
(_Azteca instabilis_). _B_, a piece of the hair-cushion with the
egg-shaped nutritive corpuscles (_nk_). After Schimper.]