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Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment

VI. The iridophores in the skin as radiation reflectors

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Summary

Hyperolius viridiflavus possesses one complete layer of iridophores in the stratum spongiosum of its skin at about 8 days after metamorphosis. The high reflectance of this thin layer is almost certainly the result of multilayer interference reflection. In order to reflect a mean of about 35% of the incident radiation across a spectrum of 300–2900 nm only 30 layers of well-arranged crystals are required, resulting in a layer 10.5 μm thick. These theoretical values are in good agreement with the actual mean diameter of single iridophores (15.0±3.0 μm), the number of stacked platelets (40–100) and the measured reflectance of one complete layer of these cells (32.2±2.3%). Iridescence colours typical of multilayer interference reflectors were seen after severe dehydration. The skin colour turned from white (0–10% weight loss) through a copper-like iridescence (10–25% weight loss) to green iridescence (25–42%). In dry season state, H. viridiflavus needs a much higher reflectance to cope with the problems of high solar radiation load during long periods with severe dehydration stress. Dry-adapted skin contains about 4–6 layers of iridophores. The measured reflectance (up to 60% across the solar spectrum) of this thick layer (over 60 μm) is not in keeping with the results obtained by applying the multilayer interference theory. Light, scattered independently of wavelength from disordered crystals, superimposes on the multilayer-induced spectral reflectance. The initial parallel shift of the multilayer curves with increasing thickness and the almost constant (“white”) reflectance of layers exceeding 60 μm clearly point to a changing physical basis with increasing layer thickness.

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References

  • Bagnara JT (1966) Cytology and cytophysiology of non-melanophore pigment cells. Int Rev Cytol 20:173–205

    Google Scholar 

  • Bagnara JT (1976) Color change. In: Loft B (ed) Physiology of the Amphibia, vol III. Academic Press, New York San Francisco London

    Google Scholar 

  • Bagnara JT, Handley ME (1973) Chromatophores and color change. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Bagnara JT, Taylor JD, Hadley ME (1968) The dermal chromatophore unit. J Cell Biol 38:67–79

    Google Scholar 

  • Bagnara JT, Frost SK, Matsumoto J (1978) On the development of pigment pattern in Amphibia. Am Zool 18:301–312

    Google Scholar 

  • Balinsky JB, Chemaly SM, Currin AE, Lee AR, Thompson RL, van der Westhuizen DR (1976) A comparative study of enzymes of urea and uric acid metabolism in different species of Amphibia, and the adaptation to the environment of the tree frog Chiromantis xerampelina Peters. Comp Biochem Physiol 54B:549–555

    Google Scholar 

  • Ballowitz E (1912) Über chromatische Organe in der Haut von Knochenfischen. Anat Anz 42:186–190

    Google Scholar 

  • Becher H (1929) Über die Verwendung des Opak-Illuminators zu biologischen Untersuchungen nebst Beobachtungen an den lebenden Chromatophoren der Fischhaut in auffallendem Licht. Z Wiss Mikrosk 46:89–124

    Google Scholar 

  • Biedermann W (1892) Über den Farbwechsel der Frösche. Arch Ges Physiol 51:455–508

    Google Scholar 

  • Bone Q, Denton EJ (1971) The osmotic effects of electron microscope fixatives. J Cell Biol 49:571–581

    Google Scholar 

  • Carey C (1978) Factors affecting body temperature of toads. Oecologia 35:197–219

    Google Scholar 

  • Connolly CJ (1925) Adaptive changes and colour of Fundulus. Biol Bull 48:56–77

    Google Scholar 

  • Cott HB (1957) Adaptive colouration in animals. Methuen, London

    Google Scholar 

  • Denton E (1970) Review lecture: on the organisation of reflecting surfaces in some marine animals. Philos Trans R Soc London Ser B: 258:285–313

    Google Scholar 

  • Drewes RC, Hillmann SS, Putnam RW, Sokol OM (1977) Water, nitrogen and ion balance in the African tree frog Chiromantis petersi Boulanger (Anura: Rhacophoridae) with comments on the structure of the integument. J Comp Physiol 116:257–267

    Google Scholar 

  • Fingerman M (1965) Chromatophores. Physiol Rev 45:296–339

    Google Scholar 

  • Fischer U (1980) Wärmereflektierendes Plexiglas. Röhm Spektrum 21:33–34

    Google Scholar 

  • Foster KW (1933) Colour changes in Fundulus with reference to colour changes of iridosomes. Proc Natl Acad Sci USA 19:535–540

    Google Scholar 

  • Foster KW (1937) The blue phase in the colour change of fish with special reference to the role of guanine deposits in the skin of Fundulus heteroclitus. J Exp Zool 77:169–213

    Google Scholar 

  • Fries EFB (1942) White pigment effectors (leucophores) in killifishes. Proc Natl Acad Sci USA 28:396–401

    Google Scholar 

  • Fries EFB (1958) Iridescent white reflecting chromatophores (antaugonophores, iridoleucophores) in certain teleost fishes, particularly in Bathygobius. J Morphol 103:203–254

    Google Scholar 

  • Fox DL (1953) Animal biochromes and structural colours. Cambridge University Press, Cambridge

    Google Scholar 

  • Fox HM, Vevers HG (1960) The nature of animal colours. Oxford University Press, Oxford

    Google Scholar 

  • Frost SK, Robinson SJ (1984) Pigment cell differentiation in the fire-bellied toad, Bombina orientalis: I. Structural, chemical, and physical aspects of the adult pigment pattern. J Morphol 179:229–242

    Google Scholar 

  • Gates DM (1980) Biophysical ecology. Springer, New York Heidelberg Berlin

    Google Scholar 

  • Geise W (1987) Leben unter Extrembedingungen: Untersuchungen zur Aestivationsphysiologie und zur Variabilität im Lebenszyklus beim afrikanischen Riedfrosch, Hyperolius viridiflavus (Annura: Hyperoliidae). Dissertation, Faculty of Biology University of Würzburg

  • Geise W, Linsenmair KE (1986) Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment: II. Some aspects of water economy of Hyperolius viridiflavus nitidulus under wet and dry season conditions. Oecologia 68:542–548

    Google Scholar 

  • Heavens OS (1960) Optical properties of thin films. Rep Prog Phys 23:1–65

    Google Scholar 

  • Huxley AF (1966) A theoretical treatment of the reflexion of light by multilayer structures. J Exp Biol 48:227–245

    Google Scholar 

  • Kobelt F, Linsenmair KE (1986) Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment: I. The skin of Hyperolius viridiflavus nitidulus in wet and dry season conditions. Oecologia 68:533–541

    Google Scholar 

  • Kortüm G (1969) Reflexionsspektroskopie, Springer, Berlin Heidelberg New York

    Google Scholar 

  • Kutchai H, Steen JB (1971) The permeability of the swimbladder. Comp Biochem Physiol 29:119–123

    Google Scholar 

  • Land MF (1966) A multilayer interference reflector in the eye of the scallop Pecten maximus. J Exp Biol 45:433–477

    Google Scholar 

  • Land MF (1972) The physics and biology of animal reflectors. Prog Biophys Mol Biol 24:75–106

    Google Scholar 

  • Menter DG, Obika M, Tchen TT, Taylor D (1979) Leucophores and iridopheres of Fundulus heteroclitus: biophysical and ultrastructural properties. J Morphol 160:103–120

    Google Scholar 

  • Nielsen HI (1978) Ultrastructural changes in the dermal chromatophore units of Hyla arborea during color change. Cell Tissue Res 194:405–418

    Google Scholar 

  • Nielsen HI, Dyck J (1978) Adaptation of the tree frog, Hyla cinerea, and the role of the three chromatophore types. J Exp Zool 205:79–94

    Google Scholar 

  • Nopp H (1964) Melanine und ihre Rolle im tierischen Organismus. Verh Zool Bot Ges Wien 103/104:16–54

    Google Scholar 

  • Odiorne JM (1933) The occurrence of guanophores in Fundulus. Proc Natl Acad Sci USA 19:535–540

    Google Scholar 

  • Porter WP (1967) Solar radiation through the living body walls of vertebrates with emphasis on desert reptiles. Ecol Monogr 37:273–296

    Google Scholar 

  • Romeis B (1968) Mikroskopische Technik. Oldenburg München, Wien

    Google Scholar 

  • Rohrlich ST, Porter KR (1972) Fine structural observations relating the production of color by the iridophores of a lizard, Anolis caroliniensis, J Cell Biol 53:38–52

    Google Scholar 

  • Schiøtz A (1967) The treefrogs (Rhacophoridae) of West Africa. Spolia Zool Mus Hauniensis 25:222–229

    Google Scholar 

  • Schiøtz A (1971) The superspecies Hyperolius viridiflavus (Anura). Vidensk Medd Dan Naturhist Foren Khobenhavn 134:21–76

    Google Scholar 

  • Shanes AM, Nigrelli RF (1941) The chromatophores of Fundulus heteroclitus in polarized light. Zoologica (N Y Zool Soc) 26:237–243

    Google Scholar 

  • Schmuck R, Linsenmair KE (1988) Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment: III. Aspects of nitrogen metabolism and osmoregulation in the reed frog, Hyperolius viridiflavus taeniatus, with special reference to the role of iridophores. Oecologia 75:354–361

    Google Scholar 

  • Schmuck R, Kobelt F, Linsenmair KE (1988) Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment: V. Iridophores and nitrogen metabolism. J Comp Physiol B 158:537–546

    Google Scholar 

  • Shoemaker VH, Balding D, Ruibal R, McClanahan LL (1972) Uricotelism and low evaporative water loss in a South American frog. Science 175:1018–1020

    Google Scholar 

  • Stahl E (1967) Dünnschicht-Chromatographie. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Tracy CR (1972) A model of water and energy dynamic interrelationships between and amphibian and its environment. PhD thesis, University of Wisconsin

  • Tracy CR (1975) Water and energy relations of terrestrial amphibians: insights from mechanistic modeling. In: Gates DM, Schmerl R (eds) Perspectives in biophysical ecology. Springer, New York Berlin Heidelberg, pp 325–346

    Google Scholar 

  • Tracy CR (1976) A model of the dynamic exchanges of water and energy between a terrestrial amphibian and its environment. Ecol Monogr 46:293–326

    Google Scholar 

  • Van Rynberk G (1906) Über den durch Chromatophoren bedingten Farbwechsel der Tiere (sog. chromatische Hautfunktion). Ergeb Physiol Biol Chem Exp Pharmacol 5:347–571

    Google Scholar 

  • Willmer PG, Unwin DM (1981) Field analyses of insect heat budgets: reflectance, size and heat rates. Oecologia 50:250–255

    Google Scholar 

  • Withers PC, Hillmann SS, Drewes RC, Sokol OM (1982) Water loss and nitrogen exretion in sharp-nosed frogs (Hyperolius nasutus: Anura: Hyperoliidae). J Exp Biol 97:335–343

    Google Scholar 

  • Wohlfarth KE (1957) Die Kontrastierung tierischer Zellen und Gewebe im Rahmen ihrer elektronenmikroskopischen Untersuchung an ultra-dünnen Schnitten. Naturwissenschaften 44:287–288

    Google Scholar 

  • Yorio T, Bentley PJ (1977) Asymmetrical permeability of the integument of tree frogs (Hylidae). J Exp Biol 67:197–204

    Google Scholar 

Download references

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Kobelt, F., Linsenmair, K.E. Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment. J Comp Physiol B 162, 314–326 (1992). https://doi.org/10.1007/BF00260758

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