Ryozo Fujii

Cytophysiology of Fish Chromatophores

Publisher Summary This chapter discusses cytophysiology of fish chromatophores, with emphasis on the chromatophores of class Osteichthyes. The chromatophores are responsible not only for the generation of color but also for changes in coloration of the surface coat. The beautiful colors and patterns and the spectacular changes in coloration is considered an important phenomena as it provides protection and assist in the survival of species in their habitats. Many poikilothermic aquatic animals, including fishes, use chromatic changes as a means of visual communication. The chapter highlights “physiological color changes,” which are the rapid changes caused by the motile activities of chromatophores. The absorption of light by the pigment in poikilothermic vertebrates is achieved by the light absorbing chromatophores, which include the melanophores, the erythrophores, and the xanthophores and also by the scattering and the reflection of light by intracellular structures, in the absence of colored materials, dependent on the presence in the skin of the light-reflecting chromatophores—namely, the leucophores and the iridophores. In the integument of fishes, pigment cells are found mostly in the dermis, where all the varieties of chromatophores can be located.

Receptor mechanisms in fish chromatophores—I. alpha nature of adrenoceptors mediating melanosome aggregation in guppy melanophores

Abstract 1. Either electrical nervous stimulation or adrenergic monoamines having alpha effects caused melanosome aggregation in guppy melanophores. 2. Some beta agonistic drugs were also found to be pigment-aggregating. 3. Various alpha adrenergic antagonists eliminated these melanin-aggregating effects. 4. On the other hand, beta adrenergic blocking agents were not effective in blocking these effects. 5. Postsynaptic adrenoceptors in melanophores which mediate pigment aggregation appear to be alpha adrenergic.

Factors Influencing Motile Activities of Fish Chromatophores

The beautiful coloration, conspicuous patterns and their spectacular changes displayed by many poikilotherms have always attracted attention. The animals themselves utilize these features as “aposematic” or “advertisement” coloration. Inconspicuous colors and patterns are conversely exploited as “cryptic” or “concealing” coloration. Many people simply appreciate these phenomena, while zoologists and physiologists can also enjoy studying them. For the animals themselves, however, such colors, patterns and reactions represent strategies of the utmost importance for the survival of individuals or of species. For example, “protective” coloration, which constitutes part of the cryptic coloration mentioned above, is useful for avoiding attacks by predators, while conspicuous displays function to frighten predators. On many occasions, delicate and subtle changes in hues and patterns are used for communication with conspecifics (cf. Cott 1940; Bagnara and Hadley 1973; Needham 1974; Fujii 1993a). These phenomena are especially highly evolved in fish among the vertebrates, and in particular among members of the class Osteichthyes. The chromatic systems of Osteichthyes have developed extraordinarily sophisticated properties during the evolution of this class of vertebrates over the course of more than 400 million years.

Control of chromatophore movements in dermal chromatic units of blue damselfish—II. The motile iridophore

Mechanisms controlling pigment movements in the melanophore of the blue damselfish, Chrysiptera cyanea, were studied. Histological observations revealed that the melanophore had three-dimensionally developed processes to envelop overlying small iridophores, and thus participated in the construction of a simple dermal chromatophore unit. Nervous stimulation, catecholamines and melatonin brought about melanosome aggregation in the melanophore. The actions of the nervous stimulation and catecholamines were antagonized by alpha adrenolytic agents. A beta adrenergic agonist, metaproterenol, adenosine and adenine nucleotides, and alpha-MSH acted as pigment-dispersing agents. These results indicate that the melanophore of the present material is controlled quite orthodoxly by adrenergic nerves and endocrines, notwithstanding the fact that it has quite a unique morphology among fish species, and that its motile rate is remarkably high.

Receptor mechanisms in fish chromatophores—II. Evidence for beta adrenoceptors mediating melonosome dispersion in guppy melanophores

1. In vitro methods for assessing melanin dispersion in melanophores are described, in which split fin preparations of the guppy, Lebistes reticulatus, were employed. 2. Acetylcholine and some current neurotransmitter suspects were ineffective in dispersing the pigment. 3. While exhibiting a melanin-aggregating action in higher concentrations, sympathomimetic monoamines in lower concentrations were found to disperse melanosomes. Such an action was more noticeable with beta stimulating drugs, some of them being solely pigment-dispersing. 4. These monoamine-induced dispersion responses were antagonized by beta adrenergic blocking agents. 5. Beta adrenoceptors in the melanophore appear to take part in the melanosome dispersion response of the cell.

Action of melanin-concentrating hormone (MCH) on teleost chromatophores

The in vitro effects of synthetic salmon melanin-concentrating hormone (MCH) on chromatophores of four teleost species were studied. In the erythrophores of the platyfish (Xiphophorus maculatus) and the swordtail (Xiphophorus helleri), and in the xanthophores and amelanotic melanophores of the medaka (Oryzias latipes), pigment aggregation took place in response to MCH even in the absence of Ca2+. In contrast to this, the leucophores of the medaka responded to MCH by the pigment dispersion but only when Ca2+ was present. The motile iridophores of the blue damselfish (Chrysiptera cyanea), which play a predominant role in coloration and its changes, were not affected by the hormone. Pharmacological studies employing various blocking agents suggest that the pigment-aggregating action of MCH is probably mediated through specific receptors possessed by the erythrophores, xanthophores, or amelanotic melanophores, while the pigment-dispersing action on the leucophores might be revealed through the receptors for melanophore-stimulating hormone (MSH).

The Blue Coloration of the Common Surgeonfish, Paracanthurus hepatus—II. Color Revelation and Color Changes

Abstract Measurements of spectral reflectance from the sky-blue portion of skin from the common surgeonfish, Paracanthurus hepatus, showed a relatively steep peak at around 490 nm. We consider that a multilayer thin-film interference phenomenon of the non-ideal type, which occurs in stacks of very thin light-reflecting platelets in iridophores of that region, is primarily responsible for the revelation of that hue. The structural organization of the iridophore closely resembles that of bluish damselfish species, although one difference is the presence of iridophores in a monolayer in the damselfish compared to the double layer of iridophores in the uppermost part of the dermis of surgeonfish. If compared with the vivid cobalt blue tone of the damselfish, the purity of the blue hue of the surgeonfish is rather low. This may be ascribable mainly to the double layer of iridophores in the latter since incident lightrays are complicatedly reflected and scattered in the strata. The dark-blue hue of the characteristic scissors-shaped pattern on the trunk of surgeonfish is mainly due to the dense population of melanophores, because iridophores are only present there in a scattered fashion. Photographic and spectral reflectance studies in vivo, as well as photomicrographic, photo-electric, and spectrometric examinations of the state of chromatophores in skin specimens in vitro, indicate that both melanophores and iridophores are motile. Physiological analyses disclosed that melanophores are under the control of the sympathetic nervous and the endocrine systems, while iridophores are regulated mainly by nerves. The body color of surgeonfish shows circadian changes, and becomes paler at night; this effect may be mediated by the pineal hormone, melatonin, which aggregates pigment in melanophores.

Receptor mechanisms in fish chromatophores. VI: Adenosine receptors mediate pigment dispersion in guppy and catfish melanophores

Using the guppy, Lebistes reticulatus, and the siluroid catfish, Parasilurus asotus , the effects of purine and pyrimidine derivatives on the movement of melanophores were studied. All the substances tested did not aggregate pigment within melanophores. Adenosine and adenine nucleotides were very effective in dispersing melanosomes within the cell, although adenine itself lacked such action. Derivatives of other purines than adenine and of pyrimidines did not disperse melanosomes. The pigment dispersion induced by adenine derivatives was specifically antagonized by methylxanthines. It was concluded that adenosine receptors are present on the melanophore membrane, which take part in the darkening reaction of fishes.

Receptor mechanisms in fish chromatophores—V. MSH disperses melanosomes in both dermal and epidermal melanophores of a catfish (Parasilurus asotus)

1. Synthetic alpha-MSH was tested for its action on dermal and epidermal melanophores of the siluroid catfish. Parasilurus asotus. 2. MSH did not produce melanosome aggregation in these melanophores. 3. It was, however, very effective in bringing about pigment dispersion in dermal melanophores. 4. Epidermal melanophores were also responsive to MSH, although the rate and the degree of the response was smaller than those of the dermal melanophores. 5. A possible role of MSH in skin color changes in vivo is discussed.

Receptor mechanisms in fish chromatophores—IV. Effects of melatonin and related substances on dermal and epidermal melanophores of the siluroid, Parasilurus asotus

Abstract 1. Melatonin was extremely effective in inducing melanosome aggregation in both dermal and epidermal melanophores of the siluroid catfish, Parasilurus asotus. 2. While precursors of melatonin, 5-hydroxytryptamine and N-acetyl-5-hydroxytryptamine, were without effects, its possible metabolites, 5-methoxytryptamine and 6-hydroxymelatonin, showed moderate action to aggregate the pigment. 3. Muscarinic cholinolytic agents, which were complete blockers of the melanin-aggregating nervous effect, had no influence in melatonin action. 4. Also, neither alpha nor beta adrenolytic agents showed an inhibitory effect on the melatonin action. 5. The conclusion is that the melanin-aggregating action of melatonin may be mediated by its specific receptors in the melanophores, and that the 5-methoxy group on the indole ring may be essential for its action.