[Footnote: Abstract of a paper "On the Nature and Functions of the
'Yellow Cells' of Radiolarians and Coelenterates," read to the Royal
Society of Edinburgh, on January 14, 1882, and published by permission
of the Council.--_Nature_.]
It is now nearly forty years since the presence of chlorophyl in certain
species of planarian worms was recognized by Schultze. Later observers
concluded that the green color of certain infusorians, of the common
fresh water hydra and of the fresh water sponge, was due to the same
pigment, but little more attention was paid to the subject until 1870,
when Ray Lankester applied the spectroscope to its investigation. He
thus considerably extended the list of chlorophyl containing animals,
and his results are summarized in Sachs' Botany (Eng. ed.). His list
includes, besides the animals already mentioned, two species of
Radiolarians, the common green sea anemone (_Anthea cereus_, var.
_Smaragdina_), the remarkable Gephyrean, _Bonellia viridis_, a Polychæte
worm, _Chætoperus_, and even a Crustacean, _Idotea viridis_.
The main interest of the question of course lies in its bearing on the
long-disputed relations between plants and animals; for, since neither
locomotion nor irritability is peculiar to animals; since many
insectivorous plants habitually digest solid food; since cellulose, that
most characteristic of vegetable products, is practically identical with
the tunicin of Ascidians, it becomes of the greatest interest to know
whether the chlorophyl of animals preserves its ordinary vegetable
function of effecting or aiding the decomposition of carbonic anhydride
and the synthetic production of starch. For although it had long been
known that _Euglena_ evolved oxygen in sunlight, the animal nature of
such an organism was merely thereby rendered more doubtful than ever.
In 1878 I had the good fortune to find at Roscoff the material for
the solution of the problem in the grass-green planarian, _Convoluta
schultzii_, of which multitudes are to be found in certain localities on
the coast, lying on the sand, covered only by an inch or two of water,
and apparently basking in the sun. It was only necessary to expose
a quantity of these animals to direct sunlight to observe the rapid
evolution of bubbles of gas, which, when collected and analyzed, yielded
from 45 to 55 per cent. of oxygen. Both chemical and histological
observations showed the abundant presence of starch in the green cells,
and thus these planarians, and presumably also _Hydra spongilla_, etc.,
were proved to be truly "vegetating animals."
Being at Naples early in the spring of 1879, I exposed to sunlight some
of the reputedly chlorophyl containing animals to be obtained there,
namely, _Bonellia viridis_ and _Idotea viridis_, while Krukenberg had
meanwhile been making the same experiment with _Bonellia_ and _Anthea_
at Trieste. Our results were totally negative, but so far as _Bonellia_
was concerned this was not to be wondered at since the later
spectroscopic investigations of Sorby and Schenk had fully confirmed
the opinion of Lacaze-Duthiers as to the complete distinctness of
its pigment from chlorophyl. Krukenberg, too, who follows these
investigators in terming it _bonellein_, has recently figured the
spectra of Anthea-green, and this also seems to differ considerably from
chlorophyl, while I am strongly of the opinion that the pigment of
the green crustaceans is, if possible, even more distinct, having not
improbably a merely protective resemblance.
It is now necessary to pass to the discussion of a widely distinct
subject--the long outstanding enigma of the nature and functions of the
"yellow cells" of Radiolarians. These bodies were first so called by
Huxley in his description of _Thallassicolla_, and are small bodies of
distinctly cellular nature, with a cell wall, well defined nucleus,
and protoplasmic contents saturated by a yellow pigment. They multiply
rapidly by transverse division, and are present in almost all
Radiolarians, but in very variable number. Johnnes Muller at first
supposed them to be concerned with reproduction, but afterward gave up
this view. In his famous monograph of the Radiolarians, Haeckel suggests
that they are probably secreting cells or digestive glands in the
simplest form, and compares them to the liver-cells of Amphioxus, and
the "liver-cells" described by Vogt in _Velella_ and _Porpita_. Later
he made the remarkable discovery that starch was present in notable
quantity in these yellow cells, and considered this as confirming his
view that these cells were in some way related to the function of
nutrition. In 1871 a very remarkable contribution to our knowledge of
the Radiolarians was published by Cienkowski, who strongly expressed the
opinion that these yellow cells were parasitic algæ, pointing out that
our only evidence of their Radiolarian nature was furnished by their
constant occurrence in most members of the group. He showed that they
were capable not only of surviving the death of the Radiolarian, but
even of multipying, and of passing through an encysted and an amoeboid
state, and urged their mode of development and the great variability of
their numbers within the same species as further evidence of his view.
The next important work was that of Richard Hertwig, who inclined to
think that these cells sometimes developed from the protoplasm of the
Radiolarian, and failing to verify the observations of Cienkowski,
maintained the opinion of Haeckel that the yellow cells "fur den
Stoffwechsel der Radiolarien von Bedeutung sind." In a later publication
(1879) he, however, hesitates to decide as to the nature of the yellow
cells, but suggests two considerations as favoring the view of
their parasitic nature--first, that yellow cells are to be found in
Radiolarians which possess only a single nucleus, and secondly, that
they are absent in a good many species altogether.
A later investigator, Dr. Brandt, of Berlin, although failing to confirm
Haeckel's observations as to the presence of starch, has completely
corroborated the main discovery of Cienkowski, since he finds the yellow
cells to survive for no less than two months after the death of the
Radiolarian, and even to continue to live in the gelatinous investment
from which the protoplasm had long departed in the form of swarm-spores.
He sum up the evidence strongly in favor of their parasitic nature.
Meanwhile similar bodies were being described by the investigators
of other groups. Haeckel had already compared the yellow cells of
Radiolarians to the so-called liver-cells of _Velella_; but the brothers
Hertwig first recalled attention to the subject in 1879 by expressing
their opinion that the well-known "pigment bodies" which occur in the
endoderm cells of the tentacles of many sea-anemones were also parasitic
algæ. This opinion was founded on their occasional occurrence outside
the body of the anemone, on their irregular distribution in various
species, and on their resemblance to the yellow cells of Radiolarians.
But they did not succeed in demonstrating the presence of starch,
cellulose, or chlorophyl. The last of this long series of researches is
that of Hamann (1881), who investigates the similar structures which
occur in the oral region of the Rhizostome jelly-fishes. While agreeing
with Cienkowski as to the parasitic nature of the yellow cells of
Radiolarians, he holds strongly that those of anemones and jelly-fishes
are unicellular glands.
In the hope of clearing up these contradictions, I returned to Naples
in October last, and first convinced myself of the accuracy of the
observation of Cienkowski and Brandt as to the survival of the yellow
cells in the bodies of dead Radiolarians, and their assumption of the
encysted and the amoeboid states. Their mode of division, too, is
thoroughly algoid. One finds, not unfrequently, groups of three and four
closely resembling _Protococcus_. Starch is invariably present; the wall
is true plant-cellulose, yielding a magnificent blue with iodine and
sulphuric acid, and the yellow coloring matter is identical with that
of diatoms, and yields the same greenish residue after treatment with
alcohol. So, too, in Velella, in sea-anemones, and in medusæ; in all
cases the protoplasm and nucleus, the cellulose, starch, and chlorophyl,
can be made out in the most perfectly distinct way. The failure of
former observers with these reactions, in which I at first also shared,
has been simply due to neglect of the ordinary botanical precautions.
Such reactions will not succeed until the animal tissue has been treated
with alcohol and macerated for some hours in a weak solution of caustic
potash. Then, after neutralizing the alkali by means of dilute acetic
acid, and adding a weak solution of iodine, followed by strong sulphuric
acid, the presence of starch and cellulose can be successively
demonstrated. Thus, then, the chemical composition, as well as the
structure and mode of division of these yellow cells, are those of
unicellular algæ, and I accordingly propose the generic name of
_Philozoon_, and distinguish four species, differing slightly in size,
color, mode of division, behavior with reagents, etc., for which the
name of _P. radiolarum, P. siphonophorum, P. actiniarum_, and _P.
medusarum_, according to their habitat, may be conveniently adopted.
It now remains to inquire what is their mode of life, and what their
function.
I next exposed a quantity of Radiolarians (chiefly _Collozoum_) to
sunshine, and was delighted to find them soon studded with tiny
gas-bubbles. Though it was not possible to obtain enough for a
quantitative analysis, I was able to satisfy myself that the gas was not
absorbed by caustic potash, but was partly taken up by pyrogallic acid,
that is to say, that little or no carbonic acid was present, but that a
fair amount of oxygen was present, diluted of course by nitrogen.
The exposure of a shoal of the beautiful blue pelagic Siphonophore,
_Velella_, for a few hours, enabled me to collect a large quantity of
gas, which yielded from 24 to 25 per cent. of oxygen, that subsequently
squeezed out from the interior of the chambered cartilaginous float,
giving only 5 per cent. But the most startling result was obtained
by the exposure of the common _Anthea cereus_, which yielded great
quantities of gas containing on an average from 32 to 38 per cent. of
oxygen.
At first sight it might seem impossible to reconcile this copious
evolution of oxygen with the completely negative results obtained from
the same animal by so careful an experimenter as Krukenberg, yet the
difficulty is more apparent than real. After considerable difficulty I
was able to obtain a large and beautiful specimen of _Anthea cereus_,
var. _smaragdina_, which is a far more beautiful green than that with
which I had been before operating--the dingy brownish-olive variety,
_plumosa_. The former owes its color to a green pigment diffused chiefly
through the ectoderm, but has comparatively few algæ in its endoderm;
while in the latter the pigment is present in much smaller quantity;
but the endoderm cells are crowded by algæ. An ordinary specimen of
_plumosa_ was also taken, and the two were placed in similar vessels
side by side, and exposed to full sunshine; by afternoon the specimen of
_plumosa_ had yielded gas enough for an analysis, while the larger and
finer _smaragdina_ had scarcely produced a bubble. Two varieties of
_Ceriactis aurantiaca_, one with, the other without, yellow cells, were
next exposed, with a precisely similar result. The complete dependence
of the evolution of oxygen upon the presence of algæ, and its complete
independence of the pigment proper to the animal, were still further
demonstrated by exposing as many as possible of those anemones known
to contain yellow cells (_Aiptasia chamæleon, Helianthus troglodytes_,
etc.) side by side with a large number of forms from which these are
absent (_Actinia mesembryanthemum, Sagastia parasitica, Cerianthus_,
etc.). The former never failed to yield abundant gas rich in oxygen,
while in the latter series not a single bubble ever appeared.
Thus, then, the coloring matter described as chlorophyl by Lankester
has really been mainly derived from that of the endodermal algæ of the
variety _plumosa_, which predominates at Naples; while the anthea-green
of Krukenberg must mainly consist of the green pigment of the ectoderm,
since the Trieste variety evidently does not contain algæ in any great
quantity. But since the Naples variety contains a certain amount of
ordinary green pigment, and since the Trieste variety is tolerably sure
to contain some algæ, both spectroscopists have been operating on a
mixture of two wholly distinct pigments--diatom-yellow and anthea-green.
But what is the physiological relationship of the plants and animal thus
so curiously and intimately associated? Every one knows that all the
colorless cells of a plant share the starch formed by the green
cells; and it seems impossible to doubt that the endoderm cell or the
Radiolarian, which actually incloses the vegetable cell, must similarly
profit by its labors. In other words, when the vegetable cell dissolves
its own starch, some must needs pass out by osmose into the surrounding
animal cell; nor must it be forgotten that the latter possesses
abundance of amylolytic ferment. Then, too, the _Philozoon_ is
subservient in another way to the nutritive function of the animal, for
after its short life it dies and is digested; the yellow bodies supposed
by various observers to be developing cells being nothing but dead algæ
in progress of solution and disappearance.
Again, the animal cell is constantly producing carbonic acid and
nitrogenous waste, but these are the first necessities of life to our
alga, which removes them, so performing an intracellular renal function,
and of course reaping an abundant reward, as its rapid rate of
multiplication shows.
Nor do the services of the _Philozoon_ end here; for during sunlight
it is constantly evolving nascent oxygen directly into the surrounding
animal protoplasm, and thus we have actually foreign chlorophyl
performing the respiratory function of native hæmoglobin! And the
resemblance becomes closer when we bear in mind that hæmoglobin
sometimes lies as a stationary deposit in certain tissues, like the
tongue muscles of certain mollusks, or the nerve cord of _Aphrodite_ and
Nemerteans.
The importance of this respiratory function is best seen by comparing
as specimens the common red and white Gorgonia, which are usually
considered as being mere varieties of the same species, _G. verrucosa_.
The red variety is absolutely free from _Philozoon_, which could not
exist in such deeply colored light, while the white variety, which I am
inclined to think is usually the larger and better grown of the two, is
perfectly crammed. Just as with the anemones above referred to, the
red variety evolves no oxygen in sunlight, while the white yields
an abundance, and we have thus two widely contrasted _physiological
varieties_, as I may call them, without the least morphological
difference. The white specimen, placed in spirit, yields a strong
solution of chlorophyl; the red, again, yields a red solution, which was
at once recognized as being tetronerythrin by my friend M. Merejkowsky,
who was at the same time investigating the distribution and properties
of that remarkable pigment, so widely distributed in the animal kingdom.
This substance, which was first discovered in the red spots which
decorate the heads of certain birds, has recently been shown by
Krukenberg to be one of the most important of the coloring matter of
sponges, while Merejkowsky now finds it in fishes and in almost all
classes of invertebrate animals. It has been strongly suspected to be an
oxygen-carrying pigment, an idea to which the present observation seems
to me to yield considerable support. It is moreover readily bleached
by light, another analogy to chlorophyl, as we know from Pringsheim's
researches.
When one exposes an aquarium full of _Anthea_ to sunlight, the
creatures, hitherto almost motionless, begin to wave their arms, as if
pleasantly stimulated by the oxygen which is being developed in their
tissues. Specimens which I kept exposed to direct sunshine for days
together in a shallow vessel placed on a white slab, soon acquired a
dark, unhealthy hue, as if being oxygenated too rapidly, although I
protected them from any undue rise of temperature by keeping up a flow
of cold water. So, too, I found that Radiolarians were killed by a day's
exposure to sunshine, even in cool water, and it is to the need for
escaping this too rapid oxidation that I ascribe their remarkable habit
of leaving the surface and sinking into deep water early in the day.
It is easy, too, to obtain direct proof of this absorption of a great
part of the evolved oxygen by the animal tissues through which it has to
pass. The gas evolved by a green alga (_Ulva_) in sunlight may contain
as much as 70 per cent. of oxygen, that evolved by brown algae
(_Haliseris_) 45 per cent., that from diatoms about 42 per cent.; that,
however, obtained from the animals containing _Philozoon_ yielded a very
much lower percentage of oxygen, e.g. _Velella_ 24 per cent., white
_Gorgonia_ 24 per cent., _Ceriactis_ 21 per cent., while Anthea, which
contains most algæ, gave from 32 to 38 per cent. This difference is
naturally to be accounted for by the avidity for oxygen of the animal
cells.
Thus, then, for a vegetable cell no more ideal existence can be imagined
than that within the body of an animal cell of sufficient active
vitality to manure it with carbonic acid and nitrogen waste, yet of
sufficient transparency to allow the free entrance of the necessary
light. And conversely, for an animal cell there can be no more ideal
existence than to contain a vegetable cell, constantly removing
its waste products, supplying it with oxygen and starch, and being
digestible after death. For our present knowledge of the power of
intracellular digestion possessed by the endoderm cells of the lower
invertebrates removes all difficulties both as to the mode of entrance
of the algæ, and its fate when dead. In short, we have here the relation
of the animal and the vegetable world reduced to the simplest and
closest conceivable form.
It must be by this time sufficiently obvious that this remarkable
association of plant and animal is by no means to be termed a case of
parasitism. If so, the animals so infested would be weakened, whereas
their exceptional success in the struggle for existence is evident.
_Anthea cereus_, which contains most algæ, probably far outnumbers all
the other species of sea-anemones put together, and the Radiolarians
which contain yellow cells are far more abundant than those which are
destitute of them. So, too, the young gonophores of Velella, which
bud off from the parent colony and start in life with a provision of
_Philozoon_ (far better than a yolk-sac) survive a fortnight or more in
a small bottle--far longer than the other small pelagic animals. Such
instances, which might easily be multiplied, show that the association
is beneficial to the animals concerned.
The nearest analogue to this remarkable partnership is to be found in
the vegetable kingdom, where, as the researches of Schwendener, Bornet,
and Stahl have shown, we have certain algæ and fungi associating
themselves into the colonies we are accustomed to call lichens, so that
we may not unfairly call our agricultural Radiolarians and anemones
_animal lichens_. And if there be any parasitism in the matter, it is
by no means of the alga upon the animal, but of the animal, like the
fungus, upon the alga. Such an association is far more complex than
that of the fungus and alga in the lichen, and indeed stands unique in
physiology as the highest development, not of parasitism, but of the
reciprocity between the animal and vegetable kingdoms. Thus, then, the
list of supposed chlorophyl containing animals with which we started,
breaks up into three categories; first those which do not contain
chlorophyl at all, but green pigments of unknown function (_Bonelia<,
Idotea_, etc.); secondly, those vegetating by their own intrinsic
chlorophyl (_Convoluta_, _Hydra_, _Spongilia_); thirdly, those
vegetating by proxy, if one may so speak, rearing copious algae in their
own tissues, and profiting in every way by the vital activities of
these.