ECOLOGICAL BIOCHEMISTRY - Study Guide - V. M. Isaienko 2005

Chapter 8. RESISTANCE AND ADAPTATION OF PLANTS AND ANIMALS

8.3. Resistance and adaptation of animals to environmental conditions

8.3.5. Changes in exterior coloration

The movement of pigments within specific Cells of the integumentary tissue or certain Organs results in changes in animal coloration. This phenomenon is observed in Protozoa (such as Euglena), Annelids, certain insects, Echinoderms, cephalopods, crustaceans, and several species of vertebrates (cyclostomes, reptiles, amphibians). Special pigment-bearing cells (Organelles) located in the Skin or deeper Tissues are called chromatophores (from Greek chroma meaning color and pharos meaning bearer). Pigment concentrated into a tiny sphere (in a granular state) has virtually no effect on the animal's overall coloration. However, when the pigment is distributed over a large surface area (in a reticular state), the coloration of the entire animal or a major part of it takes on the hue of the pigment.

Under physiological conditions, chromatophore color changes occur through the redistribution of pigment within them, driven by The ability to either concentrate or disperse it. Meanwhile, morphological changes in animal coloration are determined by variations in the total amount of pigment within the chromatophores.

Color changes in animals serve several Functions. One of these is protective coloration, which facilitates defense or attack, thereby increasing survival chances. Other functions include protection against intense illumination and thermoregulation. Additionally, color change is associated with reproduction; in certain animals—particularly specific species of lizards, cephalopods, and teleost Fishes—color alterations occur during the mating and breeding season.

Animal chromatophores exist in two main types. The first type, characteristic of cephalopods, constitutes a complex organ consisting of a pigment-containing Cell coupled with A large number (up to 29%) of radially arranged non-striated Muscle fibers. Typically, the pigment is enclosed in an elastic sac within The Cell. Upon contraction, the chromatophore fibers stretch the central cell, increasing the diameter of the resulting disc by 15–20 times. Following the relaxation of the radial fibers, the central pigmented cell resumes its spherical shape due to elasticity.

The pigments in cephalopod chromatophores belong to chromes. Their variety can differ; for instance, chromatophores containing red-brown and yellow pigments have been found in the octopus Octopus, whereas brown, red, and yellow pigments are present in the squid Loligo. Beneath the chromatophores lies a stationary layer of light-reflecting pigments, enabling cephalopod chromatophores to alter their coloration rapidly.

In most animals, unlike cephalopods, chromatophores are of a different type. They consist of either a single cell (e.g., in vertebrates) or a group of closely associated cells, or syncytia (e.g., in crustaceans). These chromatophores are highly branched, and pigment redistribution within them occurs through Intracellular Movements.

Chromatophores vary across different animals in shape, pigment type, and responsiveness to various factors. In some insects, epidermal cells perform the function of chromatophores. The brown-black pigment of these cells, located beneath a layer of yellow and green pigments, moves closer to the surface and shifts into a dispersed state. The red pigment is capable of dispersing from small spherical accumulations to form a continuous layer.

Crustaceans invariably contain yellow and red pigments, which include various carotenoids typically bound to Proteins. Furthermore, crustacean chromatophores almost always contain a white, light-reflecting pigment. Some crabs contain a blue pigment, which is a carotenoid-protein complex. Under METABOLISM/18.html">The Influence of heat and alcohols, this Water-soluble blue pigment transforms into a fat-soluble red one. In certain crustaceans (Crangon, Ligia), a black or brownish-black pigment exists in the form of ommochrome, while melanin is found in some crabs and fish.

Vertebrate chromatophores generally consist of a single cell and contain a single pigment—in most cases, melanin. Light-reflecting white pigments are also present, alongside red and yellow carotenoid pigments. A stationary layer of whitish or yellowish pigments frequently contributes to vertebrate coloration. Under the influence of various factors, other pigments, particularly melanin, can migrate into the upper layers of the epidermis, thereby coloring the animal (as seen, for instance, in Anolis lizards).

It should be noted that The rate of color change varies among animals. For example, the squid Loligo and the fish Holocentrus change color within a fraction of a second; Fundulus and Lebistes fish take a few minutes; the bullhead Amiurus, most crustaceans, and insects require several hours; while flounders, the eel Anguilla, and amphibians take several days.

The function of animal chromatophores is influenced by A number of factors. For instance, low temperatures cause darkening in amphibians (such as Hyla) and reptiles (the horned lizard Phrynosoma), whereas elevated temperatures cause whitening. Invertebrates do not exhibit a uniform response to Temperature fluctuations: in the crab Callinectes and the shrimp Palaemonetes, rising temperatures lead to whitening, whereas in the shrimp Macrobrachium, both high and low temperatures lead to darkening. In contrast, the crab Uca whitens in both scenarios. The stick insect Carausius is black at 15 °C and turns green at 25 °C.

Humidity also affects coloration in amphibians; for instance, frogs (Rana) display a dark coloration in humid environments and a light one in dry conditions.

Certain crustaceans, notably Hyperia galba, pale when attached to their host (jellyfish) and turn black when swimming freely. Thus, their coloration changes in response to tactile stimulation.

A number of animals alter their coloration in response to general excitement. For example, squids and cuticles—when agitated by the presence of a predator (such as a large crab)—change color in the form of rapid waves of color sweeping across the body surface. Similar color changes occur in these animals during the mating season.

Some reptiles, amphibians, and fish are also capable of altering their coloration when excited. Thus, the horned lizard Phrynosoma pales, the clawed frog Xenopus darkens, and the Anolis lizard becomes mottled.

Among environmental factors, light intensity has a significant impact on animal coloration. For most animals, The Effect of light is mediated through the eyes, the Central Nervous system, and various effector pathways—neural, humoral, or both. This serves as an adaptation to provide animals with protective or camouflage coloration matching their Background. For instance, the shrimp Palaemonetes can adapt its coloration against white, black, red, yellow, blue, and green backgrounds; the crabs Portunus ordvayi match white, black, red, and yellow; the cephalopods Octopus and Sepia match black, orange, and yellow; and the flounder Paralichthys albiguttus matches red, green, yellow, and blue. The ability to change color is particularly renowned in chameleons (Chamaeleo, Lophosaura, etc.).

Adaptation to background coloration is associated with corresponding pigment movements within chromatophores. Some animals exhibit the ability to alter both the distribution and the quantity of various pigments. In order for animals to distinguish background

coloration, they must respond appropriately not only to the intensity of incident and reflected light, but also to the wavelength of light.

In certain animals, daily rhythms of color change persist even when they are kept at constant temperature, humidity, and illumination. For example, crabs continue to darken during the day and pale at night for a long time when kept in total darkness. Circadian rhythms of color change have also been observed in many other crustaceans, lampreys (Lampetra), minnows (Phoxinus), salamander larvae, frogs, lizards, sea urchins, and other animals.

Let us examine the color changes in specific animal representatives in somewhat greater detail.

ANNELIDS. The coloration of certain annelids generally pales in the dark and becomes vibrant under illumination. The Mediterranean polychaete Nereis dumerilii contains red and brownish-purple pigments characterized by a circadian migration rhythm. Brown and green pigments have been identified in the duck leech Protoclepsis tessullata.

The leech Placobdella parasitica contains several types of pigments that produce its mottled white and brown coloration: pale yellow, dark greenish, and reddish-brown pigments. Notably, the function of chromatophores containing the green pigment is regulated by The Nervous System, with pigment dispersion occurring upon stimulation. Meanwhile, the content of the reddish-brown pigment changes in response to stimulation independently of the green one; its amount is variable, and it is capable of concentration.

ECHINODERMS. Color changes among echinoderms have been studied most extensively in sea urchins. For instance, Arbacia pustulosa exhibits a reddish color when illuminated (against a white and red background), whereas it turns brown when kept in the dark. The sea urchin Centrostephanus longispinus changes its color from dark purple to gray when kept in the dark for 1–2 hours. During dark adaptation, the reddish-brown pigment in these animals concentrates, whereas during light adaptation, it disperses.

CEPHALOPOD Mollusks. The function of chromatophores in cephalopods is regulated primarily by the nervous system. A color center is localized within the central ganglion, which in turn is regulated by an inhibitory center of the chromatophore system, also located in the central ganglion.

The suckers on the limbs are also capable of influencing the coloration of cephalopods—if they are removed, the chromatophores lose their tone, and the coloration becomes lighter. A similar phenomenon occurs upon the removal of the eyes. However, after the removal of both suckers and eyes, cephalopods

mollusks retain the ability to change their coloration in response to strong stimuli.

The Blood of cephalopods contains tyramine and betaine. The former, similar to adrenaline, increases the tone of motor centers, leading to darkening. Betaine, much like acetylcholine, conversely decreases tone, causing the animals to lighten. Thus, these substances act as humoral factors in the color change of cephalopods. However, humoral regulation is relatively slow. Therefore, rapid color regulation requires additional mechanisms, meaning that dual innervation exists. Evidently, the action of the muscle fibers of chromatophore cells is determined by the functioning of motor Neurons.

INSECTS. Many insects are capable of changing their coloration. The color intensity of pupae in many butterflies depends on the rearing temperature—they exhibit a darker coloration at lower temperatures. The involvement of Hormones, particularly those from the juvenile and prothoracic glands, has been established in the coloration of the pupae of the ichneumon wasp Habrobracon and the bug Perillus. The coloration of Pieris brassicae is determined by cuticle melanin, white pigment in epidermal cells, and green pigment in deeper tissues. The pupal coloration of Pieris brassicae is also influenced by the background color: they appear grayish-white on black and red backgrounds, and light green on a green background.

Four pigments have been identified in the stick insect Carausius morosus: brown, orange-red, yellow, and green. The first two concentrate and disperse under the action of external stimuli, whereas the other two show no such capability. Increased humidity also affects the stick insect's coloration, causing a darkening that reverts to lightening after 1–2 hours in dry air. In addition, illumination perceived by the eyes is of great importance: on black and red backgrounds, the Carausius stick insect has a dark coloration, whereas on white and yellowish backgrounds, it is light.

The so-called C-hormone, the deficiency of which causes the pale gray color of the insect, has been isolated from the Brain of the stick insect.

CRUSTACEANS. Most crustaceans contain white, red, yellow, and frequently also black, brown, and blue pigments. Experiments with Palaemonetes have demonstrated that the eyestalk contains a substance that causes the concentration of the red pigment and the dispersion of the white pigment, thereby paling the coloration. Removal of the eyestalk results in darkening, for instance, in Crangon and Palaemon.

Depending on the role played by the eyestalk, decapod crustaceans can be divided into three groups: Group I includes the genera Palaemonetes, Hippolyte, Orconectes, and Cambarellus, which contain primarily red, yellow, blue, and white pigments; Group II encompasses only the genus Crangon with black, brown, red, yellow, and white pigments; Group III unites the majority of crabs—Eriocheir, Hemigrapsus, Callinectes, Uca, Sesarma—which contain black, red, yellow, and white pigments.

In animals of Group I, following eyestalk removal, the red and yellow pigments disperse, resulting in darkened coloration. In Group II animals, a temporary darkening of the red telson appendages occurs simultaneously with the lightening of the rest of the body. Subsequently (after 30–60 minutes), the coloration changes: the telson and red appendages turn whiter, while the rest of the body darkens and displays a mottled coloration. Animals of Group III lighten after eyestalk removal, and most of the dark coloration becomes mottled. Thus, eyestalk hormones of crustaceans significantly influence their coloration. It should be noted that the majority of chromatophorotropic hormones are produced in neurosecretory cells associated with the eyestalks. As a rule, these hormones are distributed evenly throughout the nervous system (Palaemonetes, Cambarus, Homarus) or localized in specific areas (for example, in the posterior part of the thoracic chain in Pagurus).

In crustaceans, particularly Crangon, Uca, and Palaemonetes, hormones have been discovered that cause preferential darkening or lightening of the body or solely the tail. These hormones are of a peptide nature.

Similar to decapod crustaceans, color-change hormones have been found in isopods (specifically Sphaeroma, Idotea, and Ligia) and mantis shrimp (Squilla).

VERTEBRATES. In vertebrates possessing chromatophores, the mechanisms of color change are similar. Let us examine some of these animals.

Amphibians. During the Cytology/cytology/16.html">Early stages of amphibian development, only primary responses to light are manifested: the color is bright in the light and pale in the dark. This has been well described for young frogs of Rana pipiens and Amblystoma. In some other amphibians, notably Bombinator, Hyla, and Xenopus, secondary responses associated with visual organ stimulation predominate, although primary responses are also manifested.

Experiments with tadpoles have demonstrated that the Pituitary Gland produces hormones that regulate melanin dispersion. Removal of the posterior lobe of the pituitary gland causes the animals to lighten and lose their capacity for color change. Therefore, the hormone regulating color change in amphibians, particularly Rana, is produced by the posterior lobe of the pituitary.

Xenopus produces at least two similar hormones: one regulates melanin dispersion (melanophore-stimulating hormone), and the other regulates melanin concentration (melanin-concentrating hormone). The former is always secreted in the intermediate lobe of the pituitary upon illumination, whereas under dim light or in darkness, its release into the blood decreases. The second of these hormones responds to a black or white background and is produced in the posterior lobe of the pituitary. Notably, frog skin itself contains a melanin-concentrating factor.

Cyclic AMP is able to mimic the action of melanophore-stimulating hormone on Rana skin and is evidently a precursor to this hormone. Sodium ions are required for The stimulation of this hormone. Its indirect stimulation, leading to the darkening of Xenopus, is caused by thyroxine.

Fish. These animals contain various types of chromatophores. Black, yellow, red, and white pigments are the most prevalent. In addition, some fish contain a bluish-green pigment. In fish, as in amphibians, primary responses predominate during early developmental stages: darkening upon illumination and paling in darkness (young individuals of Perca, Salmo, Macropodus, Hoplias, etc.). In some fish, the primary response stage is weakly expressed or absent (Fundulus, Lebistes, Xiphophorus, Gambusia, Mustelus, etc.). Background responses depend on visual stimulation and the resulting Reactions of the nervous and endocrine systems. The combined action of the humoral and nervous systems is the primary regulatory mechanism of color change in fish, particularly teleosts. The presence of an adrenaline-like substance has been demonstrated in these fish, which originates from nerve endings and acts on chromatophore muscle fibers to stimulate pigment concentration. At the same time, fibers exist that stimulate pigment dispersion under the influence of acetylcholine.

In addition to dual-neuron chromatophores, single-neuron chromatophores also exist, notably in the smooth-hound shark Mustelus squalus. Under neural regulation, these stimulate pigment concentration. In other sharks, such as Raja and Scyliorhinus, as well as in the lamprey Lampetra, chromatophore innervation is not directly present. It is believed that they contain aneural chromatophores whose activity is regulated exclusively by hormones. Among fish hormones regulating chromatophore function, an important role—as in amphibians—belongs to the melanin-concentrating and melanin-dispersing hormones produced by the pituitary gland.

In teleosts, as in cartilaginous fish, the pituitary hormone involved in melanin dispersion influences coloration to a greater or lesser extent. This has been demonstrated, in particular, for the eel Anguilla and the bullhead catfish Ameiurus. Meanwhile, in the killifish Fundulus, neural regulation of chromatophores predominates: color change occurs very rapidly (1–2 min), hypophysectomy fundamentally does not affect this process, and sodium ions effectively stimulate melanin dispersion.

Considerably less is known about color changes involving other pigments compared to melanin. For instance, in the squirrelfish Holocentrus, with the participation of red pigments contained in erythrophores, the color can change from red to white within 5 seconds, and revert to red within 20 seconds when the environmental color changes from white to red and vice versa. Adrenaline induces the concentration of the red pigment. It has been established that the content of the red pigment in Holocentrus is normally regulated exclusively by the nervous system.

The Regulation of the yellow pigment found in (such as Fundulus) occurs via dual innervation, encompassing both the concentration and dispersion of this pigment. Both the nervous and humoral systems participate in this process.

Certain fish, including Fundulus and Bathygobius, contain light-reflecting white pigments localized in so-called guanophores or leucophores. The primary regulator of their function is the nervous system, although hormonal influence also occurs.

Iridophores typically contain green or blue pigments. They are sensitive to various stimuli and generally shift their color toward the red end of the spectrum upon excitation, returning to their original state once the stimulus ceases. The influence of these stimuli (such as temperature and humidity) is direct, and neither the nervous nor the humoral system is directly involved in mediating this color change.

Reptiles. Similar to fish, color change in reptiles is regulated by both the nervous and humoral systems. Initial studies on the color change of chameleons of the genera Chamaeleo and Lophosaura demonstrated the nervous system's influence on this process. However, subsequent experiments involving hypophysectomy in Anolis and Hemidactylus lizards also pointed to humoral regulation of their color changes. The color of the Anolis lizard transforms from vibrant green to dark brown. The primary reactions are darkening upon illumination and paling in the dark. When placed against a black background, color change in Anolis takes 5 — 10 minutes to complete, and the reverse transition takes 20 — 30 minutes. Following hypophysectomy, this lizard turns bright green and its coloration no longer changes against light or dark backgrounds. Darkening can be induced by administering pituitary extracts.

It has been established that melanin dispersion in Anolis is driven by the action of the melanocyte-stimulating hormone, which, as in amphibians and fish, is produced in the pituitary gland. The gradual clearance of this hormone from the blood leads to the animal's pallor. Melanin dispersion in Anolis is also triggered by cyclic AMP.

Studies on color change in iguanids of the genus Phrynosoma reveal effects similar to those found in Anolis: color regulation involves both nervous and humoral systems. These lizards darken against an illuminated black background, under very bright light, and at low temperatures. Conversely, they become pale against an illuminated white background, in the dark, and under the influence of high temperature. After hypophysectomy, Phrynosoma, much like Anolis, permanently pales. An injection of pituitary extracts induces darkening in hypophysectomized, pale-colored Phrynosoma. All of this indicates the involvement of the melanocyte-stimulating hormone in the darkening response of Phrynosoma. Evidence for the action of melanin-concentrating hormone comes from the fact that dark-colored individuals undergo bleaching when treated with adrenaline and adrenal extracts.

Unlike Anolis and Phrynosoma, color change in chameleons, particularly Chamaeleo or Lophosaura, occurs exclusively through neural regulation. Nerve transection in these reptiles causes the innervated area to darken as pigment concentrates. In intact animals, illumination causes pigment dispersion within melanophores, whereas darkness causes it to concentrate. Furthermore, alternating illumination and darkening of chameleons elicits corresponding color responses. At the same time, such reactions are absent in darkened innervated areas, indicating that humoral factors play no significant role in chameleon color change.