Plant Pigmentation and Animal Coloration

PLANT PIGMENTATION and animal coloration (its biological significance). Animal coloration has great biological significance. At various times it has been assessed differently. For the first time, the doctrine of the biological significance of coloration was put forward and developed by Darwinism, which evaluated all features useful to the animal that could be fixed and developed through selection. In particular, Wallace analyzed, classified, and grouped the facts relating hereto. Charles Darwin himself studied coloration extensively as a secondary sexual characteristic, attributing its development to the action of sexual selection. Followers of Darwin and Wallace showed a tendency to attribute every coloration of animals to usefulness without observing due caution. At the end of the 19th and the beginning of the 20th centuries, a strong anti-Darwinian movement in Western science could not fail to touch upon the question of coloration. The study of the physico-chemical side of the phenomenon was advanced, verification experiments on the significance of coloration were set up, and the opposite opinion became widespread: any coloration is useless, being merely a consequence of physical and chemical processes in or on the body of the animal. The experiments set up often gave and give a negative answer to the question of the supposed biological significance of coloration. This happens, firstly, from an underestimation of all the complex conditions of the experiment, and secondly, even more so from completely incorrectly drawn conclusions from them (see below). The biological significance of coloration is great, insofar as the dependence of animals on enemies with perfectly developed organs of vision (birds, mammals) is great, insofar as their dependence on prey that spots its pursuers is great, insofar as gregariousness plays a role in their lives, forcing the young to follow the elders for safety, and insofar as coloration facilitates the possibility for the sexes to find each other and come into appropriate arousal, contributing to more energetic reproduction. Different types of animal coloration according to their significance can be divided into two groups: 1. Coloration that plays a role in the relationship of enemies and prey to each other, i.e., helping the prey to escape from the predator and allowing the predator to imperceptibly master the prey—what the Germans call Schutzfarben or Schutztrachten (protective coloration). 2. Coloration that plays an auxiliary role during mating—Paarungstrachten. Coloration having biological significance can a) in color or pattern match the coloration of the external environment and thus make the animal imperceptible; it is useful to both the pursued animal and the pursuer—concealing or protective coloration; b) on the contrary, it can sharply single out the animal, drawing attention to it—striking coloration. Protective coloration can make the animal imperceptible, especially at a distance, when the main tone of the coloration merges with the surrounding environment. Such are: the white coloration of polar animals (white hare, fox, bear, owl, gyrfalcon), the grayish-yellow coloration of numerous animals, birds, reptiles, insects, and spiders of the desert, the green coloration of animals of tropical forests, the lack of coloration and transparency of pelagic marine animals, etc. Coloration becomes even more concealing when it conveys not only the main background, but also the pattern. There are butterflies that perfectly copy the pattern of the tree trunk on which they sit. The granular pattern of sand is reproduced on the surface of the desert-dwelling toad-headed agama. According to Vosseler, orthopterans of the African deserts convey on their elytra not only the coloration but also the structure of the soil; forms living on reddish soil take on a red tint, those living on sand take on a yellow one and have a fine-grained pattern; in insects living on pebbles, the coloration darkens and acquires a coarser granular character. The similarity goes even further if the animals adopt not only the pattern but also the form of the object on which they sit. This includes the well-known examples of the Kallima butterfly, which in a sitting position with folded wings reproduces the shape and pattern of a withered leaf with its veins, and the outgrowths of the hind wings rest against the twig where the animal sits, copying the leaf petiole. Our small tortoiseshell butterfly with folded wings also has the appearance of a dried leaf. This also includes various stick insects and mantises that reproduce the shape of twigs or leaves. Some of the tropical mantises resemble flowers in color and shape to such an extent that some butterflies and other insects sit on them and become their victims. Many caterpillars of geometrid moths reproduce the twigs of a shrub with great precision. Such similarity, usually called mimetic coloration, is aggravated by the behavior of the animal. Insects mimicking dead objects are characterized by immobility. Disturbed, they freeze for a long time in certain poses. Thus, geometrid caterpillars stretch out at an angle to the branch where they sit, holding onto the branch with only two pairs of hind legs and completely mimicking a dry twig sticking out to the side. Nekrasov observed how Crimean mantises, resembling leaves dried on petioles, swayed slightly on their thin legs in the wind, reproducing the trembling of foliage from the wind. They repeated the same movement when planted between two window frames where a strong draft blew. Weismann recounts that he once found a pine moth (Xylina) on a fence near the ground. He picked it up, examined it, took it for a piece of rotten bark, and threw it down. Then he doubted and picked it up again. It was indeed a butterfly, which did not betray itself with a single movement. P. Yu. Schmidt showed that stick insects (phasmids), the similarity of whose body and legs to twigs is especially great, can fall into a true state of catalepsy, adopting a resting posture with legs and antennae extended forward and muscles tensed. At this time, one can take one or the other leg with tweezers and give the insect any pose. It freezes in the most inconvenient poses and stands motionless for hours. One can even cut off its abdomen, segment by segment—it does not emerge from the state of catalepsy and does not make a movement. When similarity to an inanimate object reaches such a degree, one does not have to say that the similarities of mimetic coloration are accidental and owe themselves to phenomena of convergence or orthogenesis, as some anti-Darwinians want to present it. Examples of protective and mimetic coloration are so numerous, animals so often have to search for prey (as a flock of tits searches every bush in winter or autumn), that any adaptation that makes prey less noticeable, reducing the likelihood of its discovery, is vital and must be fixed by selection. Therefore, even individual experiments (among them we note those confirming the theory of protective coloration by Chesnol, who tied mantises to plants of the same color and to plants of a different color where they caught the eye, and Poulton's observations on butterfly pupae, some of which were against the background of the same color, others against an unsuitable background) do not have important significance in themselves. In particular, one must resolutely object when individual experiments and observations are cited against the protective significance of protective coloration, stating that protective coloration did not achieve its goal here or there, that the enemy noticed the prey "anyway" and that therefore the coloration has no significance. To give such an interpretation is not to understand the course of the process. Both the methods of defense and the methods of recognition and mastering prey develop in parallel. "I usually ask," Prochnov says not without wit on this occasion, "is it really because hares are caught by foxes that the speed of their legs has no significance?" Is it really—let us add—that the coloration of guns to the color of the soil, of warships to the color of the sea, of military uniforms to green or dusty "protective" colors in recent wars had no significance, since guns, ships, and people were destroyed despite them.—"The judgment of the extent to which an insect is protected," Prochnov says, "requires an investigation of the behavior and lifestyle of the insectivore and a study of the role this insect plays in the nutrition of the insectivore compared to other prey, taking into account their relative frequency." All this poses before us the problems of quantitative accounting in nature of insects, the methodology of which is still being developed. Striking coloration, drawing attention to itself, can have various meanings. First of all, it can be warning coloration. Animals possessing a sting, poisonous hairs, an unpleasant taste or smell, inedible animals are often distinguished by a bright coloration that saves them from attack. Each attempt of an inexperienced predator to attack such an animal is imprinted in its memory, and the unpleasant sensation is associated with the bright coloration. Next time it will not repeat such an attempt, and a significant number of animals with such coloration will be saved at the cost of the few victims necessary to develop the association. In stinging insects, a combination of black and yellow rings or spots is particularly common. A typical example of warning coloration in mammals is the rather striking white and black attire of the American skunk, which is distinguished by an incredibly strong and repulsive odor. Here, too, a very large number of experiments were carried out, yielding a rather mottled picture.

Of course, warning coloration, just like protective coloration, has only a relative, not an absolute significance, greatly reducing the percentage of those that perish. In general, experiments with insectivores confirm that the warning coloration of insects deters a certain number of insectivores from them. A special category of coloration is represented by the so-called intimidating coloration, usually combined with some sort of movement. Thus, in the eyed hawkmoth (Smerinthus ocellatus), the upper wings represent an example of typical dark protective coloration, but if the butterfly is disturbed, it makes a sharp movement with its body and wings, rising on its legs and immediately revealing bright red lower wings with eyespots. These "eyes", which suddenly appear before the pursuer, are attributed an intimidating significance. The same suddenly appearing eyespots are found in the caterpillars of certain hawkmoths (Chaerocampa elpenor, Leucorhampa ornatus), accompanied by the swelling of the corresponding segments, and sometimes by serpentine movements. The doctrine of intimidating coloration was especially developed by Günther in Germany and Fausek in our country. However, it has been subjected to much justified criticism (Nikolsky), and the number of cases relating to it is hardly large. The examples given above are essentially close to the third category of striking colorations, bearing the name of mimicry in the narrow sense of the word and which could be called false-warning coloration. In addition to those mentioned, there is yet another category of conspicuous colorations. This is recognition coloration, or recognition marks, clearly visible even at a distance in gregarious animals, e.g., the white raised tail of a rabbit, white patches on the rump in a whole series of gregarious mammals (antelopes, deer, fallow deer, chamois), etc. According to the interpretation of Wallace, who drew his attention to this phenomenon, the white tail or white patch on the rump of a leading animal that has started to run serves as an indicator or signal for all the younger and weaker ones, which, under the guidance of older, more experienced leaders, can sooner reach a safe place. Birds that keep in flocks are distinguished by the same, often slight recognition marks even with a general protective coloration, having white stripes or marks on the breast, head, neck, eyes, wings, tail feathers, etc. Spots on the wings and tail are often revealed only during flight. Recognition marks can also play a role in the sexual period, helping the sexes find an individual of the opposite sex of the same species. This is how some explain the vivid bright coloration of insects, especially butterflies, visible during their flight. However, the question of whether insects see colors has long aroused controversy. Hess, for example, completely denied the ability of bees to see colors, but the experiments of Prochnow and Frisch definitely prove the perhaps limited color vision of bees. In any case, many insects find the opposite sex more by scent or by sounds produced by the other sex than by coloration. Very large disputes arose about the significance and origin of coloration that is a secondary sexual characteristic, i.e., peculiar to one sex. Darwin attributed its origin to sexual selection.

Plant coloration. Biological significance in plants is held by the bright coloration of fruits and flowers. The bright coloration of flowers rich in nectar ensures their cross-pollination by means of insects (Frisch, by "training" bees to a specific color, proved that they distinguish it), while the attractive and alluring colors of the fruits of fruit trees draw the attention of frugivorous birds and animals that seek out and eat them. At the same time, the seeds of the fruits or stones pass undigested through the body of the animal and then fall into the most favorable conditions for germination. The fact that bright coloration is indeed useful for the plant and can be regarded as the result of the activity of natural selection is evident from the fact that such coloration appears no earlier than the ripening of the fruit, i.e., only when the seeds have already reached full maturity and the capacity for germination. Seeds and nuts, which are digested by the animals eating them, are usually colored green on the plant with a protective color, and fall to the ground having turned brown.

^A- Nekrasov. Development of coloration. Changes in animal coloration associated with age, sex, habitat, and various influences have been subjected to experimental investigation many times. However, despite the large number of works devoted to this question, the essence of the process of coloration development remains insufficiently clarified to this day. The study of coloration development was carried out along the line of clarifying those factors external to the pigment formations that influence the appearance, disappearance, and change of coloration. In relation to pigment tissue or pigmented derivatives of the epidermis, external factors include not only the surrounding temperature, humidity, illumination, etc., but also influences originating from other parts of the organism (nervous, humoral impulses, etc.). The convenience of systematizing the extensive factual material forces one to conventionally attribute the latter type of influences to the group of so-called internal factors, since their source is localized within the organism. Influence of light and soil coloration. Cunningham studied the coloration of flounder (Pleuronectes platessa). An adult fish lying motionless on its side has dark coloration only on the right, upward-facing side. By placing young flounder in an aquarium with a glass bottom illuminated from below, Cunningham achieved the appearance of pigmentation on the left, usually uncolored side. In animals deprived of light under normal habitat conditions, coloration is often absent. The effect of light on proteus (Kammerer) and the mollusk Lithodomus causes them to form pigment. Kammerer placed the fire salamander (Salamandra maculosa) in terrariums with differently colored soil (black and yellow). When kept on a yellow background, the amount of orange-yellow pigment increased at the expense of the black, while black soil had the opposite effect. Kammerer's data have been confirmed by Přibram and Herbst (Pribram, Herbst). The influence of a colored background or colored light rays on the coloration of butterfly pupae was studied by Dürken, Breker, and Vladimirsky. All the aforementioned authors established that in light and under the influence of a light background, the coloration of pupae becomes lighter. The necessity of sunlight for the occurrence of green coloration in plants, which depends on the presence of chlorophyll, follows from the fact that in darkness plants produce almost or completely white (etiolated) shoots. Influence of food. The coloration of the abdomen in Drosophila, determined by the abnormal-abdomen gene, depends on the nature of the food, manifesting in varying degrees of expression of transverse stripes. Some authors fed caterpillars of the geometrid with hawthorn leaves, the branches of which were standing in a solution of lead or manganese salts, and obtained darker than usual butterflies. The same result was obtained if caterpillars were given leaves taken from an industrial area, carrying a deposit of metal salts. Influence of temperature and humidity. The influence of changed temperature on butterfly coloration was established by Dorfmeister (Dorfmeister, 1864). As a result of many years of experiments, Standfuss and Fischer showed that raising pupae of the tortoiseshell butterfly and other butterflies at both high and low temperatures leads to the appearance of more darkly pigmented butterflies. The coloration of flowers of the Chinese primrose (Primula sinensis) is in close dependence on temperature and humidity. At normal temperature and moderate humidity, the flowers are colored red. An increase in temperature and humidity leads to the appearance of white flowers. The combined action of elevated (up to 35°) temperature and lack of moisture in Tower's experiments led to a change in coloration of the Colorado potato beetle (Leptinotarsa decemlineata). Experiments on some mammals are of great importance for understanding the processes of coloration development. Schulz (Schulz, 1915) showed that ermine rabbits change their coloration under the influence of temperature. White fur on the side or back after shaving and placement in conditions of low temperature is replaced by black (fig. 1). These data have been confirmed by L. Kaufman and thoroughly investigated by Ilyin, who showed that the black coloration of the ears, nose, tail, and extremities in ermine rabbits also depends on temperature. The keeping of rabbits with plucked black fur in conditions of high temperature leads to the replacement of black hairs with white ones (fig. 2). These phenomena depend on the difference in the thresholds of irritation of various parts of the body to temperature effects. The normal coloration of the ermine rabbit is also the result of the response of pigment-forming elements of the skin to temperature effects. In addition to ermine rabbits, similar reactions are given by guinea pigs, so-called Castle albinos with similar coloration, Siamese cats, and probably some other animals. The ability of Castle albino guinea pigs to respond to temperature effects allowed Ilyin to solve the question of their genetic constitution, i.e., to establish whether they are true albinos possessing the a gene, or they are similar to ermine rabbits and have the constitution A¹. Genetic analysis in this case was impossible, since completely white guinea pigs are not encountered, and both genes a and A¹ are recessive to the main coloration gene A. Analysis of the temperature response showed that Castle albino guinea pigs are not true albinos of the a type, but carry the A¹ gene similar to ermine rabbits. Influence of the nervous system has been studied insufficiently. There are data that cutting peripheral nerves leads to discoloration of the corresponding part of the body in fish. On the same object, the influence of visual sensations has been shown. These materials to a greater extent relate to the physiology of the pigment system than to the analysis of coloration development. Hormonal influences. Thyroid gland. The influence of the thyroid gland on animal coloration was studied by means of inducing artificial hyperthyroidism. Placing aquatic animals in a suspension of thyroid gland preparations or administering it to terrestrial animals orally or parenterally cannot claim to imitate the corresponding physiological and pathological phenomena. All the more, experiments with artificial hyperthyroidism are unable to solve the question of the role of this gland in coloration development. At the same time, the data presented below allow establishing the fact of hormonal influence on coloration and approaching the clarification of the essence of the processes of its development. A number of authors established that feeding chickens with thyroid gland substance or its preparations leads to molting and then to a change in coloration of the newly growing feathers. Thus, B. Zavadovsky, Giacomini, and others established the fact of partial, sometimes far-reaching depigmentation of black chickens (fig. 3), whereas Crew, on the one hand, and Torrey and Horning, on the other, noted in Wyandottes an intensified formation of black pigment. M. Zavadovsky and R. Belkin in experiments with hyperthyroidism in pheasants showed that the nature of the change in coloration depends on the amount of thyroid gland preparation administered (fig. 4a and 4b). Apparently, the different results of the experiments of the aforementioned authors must be attributed to different dosages of the thyroid preparation. The possibility of depigmentation of mammals in hyperthyroidism was initially denied. Recently, Ilyin (1931) succeeded in achieving depigmentation in rabbits by administering thyroid gland preparations. Figure 1. Influence of low temperature (around 0°) on the coloration of fur in an ermine rabbit. Growth of black hairs instead of white ones on the back and croup. (After Ilyin.) Figure 2. Growth of white hairs instead of black ones on the base of the ears of an ermine rabbit under the influence of high temperature (around +30°). (After Ilyin.) Fig. 3. Influence of hyperthyroidism on the plumage coloration of pheasants. On the right-normal male pheasant. On the left-male pheasant with depigmented plumage after feeding with thyroid gland preparation. (After Zavadovsky and Belkin.) Figure 4. On the right-tail feather of a normal pheasant (male). On the left-similar feather of a pheasant after feeding with thyroxine. Result of the experiment-hyperpigmentation (dark stripes wider). (After Zavadovsky and Belkin.) Figure 5. Normal amblystoma. Medium-sized white spots appearing during metamorphosis under the influence of thyroid gland preparations. (After Vorontsova.) Figure 6. Amblystoma obtained from an axolotl under the influence of injections of pituitary gland preparation; white spots completely absent. (After Vorontsova.) Figure 7. Tadpole Rana aurora Dratonyii-normal; dark coloration. (After Smith.) Figure 8. Tadpole Rana aurora Dratonyii, depigmented as a result of early removal of the pituitary gland; 'silvery' coloration. (After Smith.) Figure 9. On the left-normal axolotl of the black race. On the right-black axolotl, depigmented as a result of pituitary removal. (After Blyakher.) Figure 10. On the left-normal white axolotl, in the middle-normal black axolotl, on the right-white axolotl, hyperpigmented as a result of implantation under the skin of several pituitary glands from axolotls. (After Vorontsova.) Figure 11. Photomicrograph of a flat preparation of skin from a normal black axolotl. Pigment cells in a state of expansion. (After Vorontsova.) Figure 12. Photomicrograph of a flat preparation of skin from a hypophysectomized black axolotl. A distinct contraction of melanophores is noticeable. (After Vorontsova.) Figure 13. Photomicrograph of a flat preparation of skin from a normal white axolotl.

There are few pigment cells, but all of them are in a state of expansion. (According to Vorontsova.) (For illustration to the article Coloration.) See article Coloration. of the growth of white or pale-colored hairs on the ears of an ermine rabbit at low t° after feeding thyroid tablets. In control animals, the coloration of the ears remained black. On the contrary, removal of the thyroid gland in an ermine rabbit and Siamese cat led to hyperpigmentation. Thus, at t° 34°, black hairs grow again in place of the removed black hairs on the ear, whereas in unoperated animals, even at t° +25-27°, the black hairs on the ears are replaced by white ones. Ilyin interprets his results as a consequence of a change in the threshold of skin irritation to temperature irritation. (In hyperthyroidism, the irritation threshold is lowered, in thyroidectomy it is raised.) In amphibians, hyperthyroidism also leads to a change in coloration. The axolotl, which has a solid black-brown coloration, when transformed into an amblystoma usually becomes covered with white spots (fig. 5). The coloration of the axolotl is connected with the activity of the pituitary gland. Vorontsova's work showed that depigmentation in hyperthyroidism depends on a mosaic increase in the threshold of skin irritation in relation to the pituitary hormone. The simultaneous effect of a thyroid gland preparation and pituitary gland leads to the appearance of completely black amblystomas (fig. 6).-(The influence of sex hormones on coloration and the influence of thyroid hormone on sexual color characteristics-see Sex.) Pituitary gland. The influence of the pituitary hormone on the coloration of amphibians has been studied in great detail. Removal of the pituitary gland anlage in frog embryos led to the appearance of decapitated tadpoles (fig. 7). A similar operation in axolotl and newt frogs (Hogben, Blyakher) also resulted in depigmentation (fig. 8). This result is a consequence of the contraction of black pigment cells (melanophores) and a decrease in their number (fig. 9). Reverse implantation of the pituitary gland leads to complete restoration of coloration, the slower the greater the time that has passed since hypophysectomy. The white race of axolotls has a significantly smaller number of pigment cells than the black one. The matter here is not in the reduced activity of the white race, but, as Vorontsova showed, in the reduced susceptibility of the skin of the white axolotl to the action of the pituitary hormone. Implantation of several additional pituitary glands into a white axolotl leads to significant darkening, especially of the head and part of the back (fig. 10). The number of pigment cells at this time increases unusually. From Vorontsova's experiments it follows that the difference in coloration of the two races of axolotls is based not on a difference in the formative activity of the pituitary hormone, but on a difference in the properties of the skin. The coloration of amphibians is affected by adrenaline in a very distinct way. Lieben and then Vorontsova showed that the melanophores of amphibians respond to adrenaline injections with a sharp contraction, which, however, does not last long. A similar effect of adrenaline is not limited to amphibians; the melanophores of fish react to adrenaline in a similar way. In the vermillion-spotted newt (Diemyctibus viridescens), Collins and Adolf did not detect the usual contracting effect of adrenaline on melanophores. This amphibian is generally distinguished by peculiarities of pigment reaction. Injection of pituitrin causes contraction, and not expansion, of melanophores in it. The reaction of expansion of pigment cells to the introduction of pituitary hormone can also be caused by a number of other irritants. Vorontsova showed that intraperitoneal injection into hypophysectomized axolotls of emulsions from various organs (muscle, brain, etc.), as well as various organic (fibrin, peptone, glucose) and even inorganic substances (NaCl solution) causes darkening of the skin due to expansion of pigment cells. The effect of the listed substances in vitro on surviving pieces of skin also leads to expansion of melanophores. The pituitary hormone is thus not a specific irritant for the pigment system of amphibians. There are a number of substances that act on melanophores with varying degrees of intensity; the pituitary hormone is still ahead in terms of strength of action. Allen's data on the differential study of individual lobes of the pituitary gland in relation to their influence on the coloration of amphibians boil down to establishing the fact that the active principle is produced in the cerebral and possibly in the intermediate part of the gland. The mechanism of coloration change under various hormonal influences is insufficiently studied. This especially applies to birds, in which pigmented epidermal formations (feathers) have a very complex structure. In amphibians, the contraction of melanophores probably depends on the migration of melanin granules from the processes to the center of the pigment cell. The star-shaped form of the cell is preserved in this case. On the contrary, during expansion, melanin granules fill the processes of the melanophore. The deep depigmentation of amphibians after removal of the pituitary gland is apparently connected with the breakdown of pigment cells and with the release of melanin grains, which pass into the peripheral layers of the skin and are removed during molting. This process is very clearly observed in hypophysectomized toads and Spanish tritons (Pleurodeles Waltlii) (Blyakher). The mechanism of the development of coloration in many animals is still not sufficiently clear. The striped and spotted coloration of mammals, the bright coloration of birds and insects, the extraordinary examples of adaptive coloration have received a clear interpretation in the aspect of the history of the species, but have not been studied at all from the point of view of the mechanics of individual development. The attempts made in this regard by Haecker cannot yet be considered successful. (On the inheritance of coloration-see Drosophila, Rabbits, Mice.) l. Blyakher.