Abstract: Squamate epidermatoglyphics are proposed
to function as an aid in capture, dispersal and retention of pheromones.
Snakes, lizards and amphisbaenians - hence all squamate reptiles - are famed for the elaborate microornamentation of the epidermis, visible under high magnification with light microscopes (Picado, 1931) but more dramatically evident with scanning electron microscope magnifications of up to several thousand diameters (Cole and Van Devender, 1976). The configurations vary from mostly longitudinal ridges, as seen most abundantly in snakes (Picado, 1931) and burrowing lizards and amphisbaenians, to spinules and pits as in scansorial and cursorial lizards such as Sceloporus (Burstein, Larsen and Smith, 1974). Figs. 1-4 illustrate 15 species never before depicted. The patterns vary greatly and have been thought to be species-specific, hence useful clues to phylogeny (Burstein et al., 1974; Price, 1982), although Cole and Van Devender (1976) revealed evidence that intraspecific variation is far too great to permit epidermatoglyphics to be a useful tool taxonomically or phylogenetically. That particular problem remains to be elucidated: the conclusions of Burstein et al. and Price cannot be so lightly dismissed, for they took pains to eliminate factors that might be responsible for intraspecific variation. It is likely that future studies will restore credibility to epidermal microglyphics as clues in systematics.
Quite aside from the possible systematic significance of epidermatoglyphics, a question of function exists and has never been satisfactorily resolved. Many possibilities have been suggested, conspicuous among them being a mechanical facilitation for ecdysis (Maderson, 1970), since squamate reptiles are unique not only in possession of epidermatoglyphics but also in being the only vertebrates with an essentially glandless skin, the upper keratinized layers of which are molted intact or in large pieces at frequent intervals. The microornamentation might well facilitate the molting process in some way, although just exactly how remains uncertain.
Creation or minimization of friction, in accordance with the habitat and behavior of the animals, has also been proposed (Stewart and Daniel, 1973). The spinules and pits might advantageously increase friction for crevice-dwelling reptiles, as most squamates are, at least when taking refuge or when somnolent. The longitudinal ridges characteristic of limbless or near-limbless squamates might facilitate movement or removal of surface debris.
Conversion of harmful solar radiation to heat has likewise been suggested (Porter, 1967), the fine irregularities serving as a diffraction grid. Similarly, the structures might be useful in light refraction, producing iridescent colors (Monroe and Monroe, 1967). There is another possibility we here propose for the first time, and for which there is more circumstantial evidence than exists in support of any other hypothesis: that the microglyphics serve in the dispersal and retention of pheromones produced by scent glands and through epidermal capillaries between scales.
Squamate reptiles have seemingly the most efficient vomeronasal olfactory sensory system in vertebrates (Burghhardt, 1970: Duvall, King and Graves, 1982; Madison, 1977). That system is a vital means of discrimination of food and in communication, both intra-and interspecific (Chiszar et al., 1980; Duvall, 1979, 1982a, 1982b; Duvall et al., 1980; Kubie, Vagvolgyi, and Halpern, 1978). Sight, hearing, tactile and taste senses are developed in squamates to different degrees in different taxa, and in given groups one or more may be very acute, but no sensory system is so well developed across the board in squamates as the vomeronasal olfactory system, activated primarily by the tongue. In no other vertebrates is the tongue used so liberally in sampling the environment, and that attribute extends to all members of the Squamata.
Certainly vomeronasal olfaction is equally as important as vision in social communication, and perhaps more so, among squamates (Burghardt, 1980).
Yet squamatans (individual squamate reptiles, as opposed to collective groups) are exceptionally impoverished in glandular sources for pheromones, since they lack the generally distributed skin glands so characteristic of fishes, amphibians and mammals. Other reptiles and birds are similarly handicapped, but communication is facilitated in birds by exceptionally acute vision, whereas reptiles other than squamates rely heavily on senses other than olfaction for communication. They have not, incidentally, been particularly successful groups as compared with others, with but a single species of rhynochocephalian, some 23 of crocodilians and 250 of turtles, as compared with some 5750 squamate species and 8750 birds.
The only well-developed scent glands remaining in squamatans are two cloacal derivatives housed in the base of the tail in both sexes. In only a few groups are there possible pheromonal glands about the chin (some natricine snakes) and on the head generally (scolecophidians). For the bulk of, if not all, squamatans, the only pheromonal source available to them is the cloacal glands. We regard femoral and preanal pores, the escutcheon and supraanal tubercles as dispersal, not pheromonally secretive, structures.
Yet behavioral studies show that pheromones are present on the body surfaces generally, and that they are lost after each molt, being replaced shortly thereafter (e.g., Kubie, Cohen, and Halpern, 1978). It seems highly likely that the epidermatoglyphics so characteristic of squamates serve to both disperse (by capillary action facilitated by their small size) and retain pheromones between ecdyses. Presumably body movements aid in spreading the pheromones produced by the anal glands over body surfaces.
The recently documented exudation of pheromones, particularly those related to reproductive state (Duval, Guillette and Jones, 1982:212) through the capillaries between epidermal scales (Garstka, Camazine and Crews, 1982) provides another source of olfactory material retained in place by the epidermatoglyhphics. A possible extreme adaptation facilitating integumentary diffusion exists in some Indian snakes noted by Malcom Smith (1943) as having extensive bare skin overlying paired "nuchal glands" in the nape region, where chin-rubbing commonly focuses in courting snakes. Maderson (1965) gave an excellent account of the shedding cycle in squamates. The lacunar layer of the epidermis separated the old epidermal generation from the new. This layer contains many large vacuoles which
Jackson and Sharawy (1978) have shown to be filled with lipids and incorporated into the alpha-layer as it matures. These lipids also could be deposited on the outer layer of the new generation as proteolytic enzymes break down the lacunar layer in preparation for ecdysis. These may be the lipids that Warburg (1966) observed on the surface of the b -layer (i.e. Oberhautchen?).
Maderson et al. (1978) have shown the a -layer to be essential for restricting cutaneous water loss in reptiles, presumably, because of lipids present in that layer, as supported by Roberts and Lillywhite's (1980) findings that skin lipids are the determining factor in cutaneous water loss rates, because of lipids present therein. Oldak (1976) found that the odorous part of cloacal gland secretions are lipids which differ between groups and are chemically stable for over two years.
All of the above provide solid evidence for presence of lipids in and on squamate epidermis. There is also evidence for these lipids serving pheromone function. Kubie, Choen, and Halpern (1978) have shown that estradiol benzoate treated female garter snakes (T. radix) are more sexually attractive after shedding and that this sexual attractiveness is transferred to penmates. This pheromone may be lipids released from lacunar vacuoles during shedding. However, Garstka and Crews (1981) showed that the sexual attractiveness pheromone in garter snakes (T.sirtalis) is a lipid which moves through the skin.
These lines of evidence appear to us to suggest very strongly that the function of squamate epidermatoglyphics is to aid in dispersal and retention of pheromones between molts. The acutely sensitive vomeronasal system of these reptiles makes such a function tenable, whereas in less sensitive vertebrates that function would be very unlikely simply because the requisite discriminatory ability is not there. Circumstantial evidence of a functional role in pheromone capture outweighs all evidence supporting other hypotheses.
Scanning electron microscope (SEM) photographs of selected lizard scale surfaces. A = Cnemidophorus bacatus, x1900; specimen number not recorded; note numerous pits. B = Sceloporus formosus, x5000; specimen number not recorded; note profuse spicules bordering pits. C = S. scalaris, x5000; specimen number not recorded; note short spicules on ridges bordering pits.
SEM photographs of selected snake scale surfaces. A = Anilius scytale, x5000; KU 121835; Price (1982) called this an echinate pattern. B = Rhinophis drummondayi, x5000; KU 37714; another unusual pitted pattern. C = Stenorrhina freminvillei apiata (from Yucatan), x5000; KU 70892; another echinate pattern. D = Tretanorhinus nigroluteus, x2000; KU 75759; a plicate pattern similar to that of Liodytes alleni (Price, 1982).
SEM photographs of selected snake scale surfaces. A = Nerodia sipedon sipedon, x5000; KU 17757; a canaliculate pattern with crosshatching ribs very similar to Price's (1982) illustration for Nerodia fasciata. B = Lacicauda laticauda, x1000; KU 94559; another plicate pattern. C = Pelamis platurus, x2000; KU 125502; plicate like the proceeding. D = Micrurus spixi, x5000; KU 130262; echinate, much like Pseudohaje nigra (Price, 1982).
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Department of E.P.O. Biology (Hobart M. Smith and Richard E. Jones) and Department of Psychology (David Chiszar) University of Colorado, Boulder, Colorado 80309
Department of Physiology and Zoology (David Duvall and Brent M. Graves) University of Wyoming Laramie, Wyoming 82071
Published in the Bulletin of the Philadelphia Herpetological Society, Vol. 30 (1982) and Vol. 31 (1983-4 photos)