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Surface morphology of dorsal scales of red cornsnakes (Pantherophis guttatus) and gray ratsnakes (Pantherophis spiloides) from Middle Tennessee.

Abstract--We used scanning electron microscopy to characterize microornamentation of dorsal scales from the neck and midbody of two species of sympatric New World Ratsnakes (Pantherophis guttatus and Pantherophis spiloides) from middle Tennessee. The outer, beta keratin-rich layer of the squamate epidermis bears intricate fine sculpturing (microornamentation), which varies from base to apex of an individual scale. Various functions have been attributed to microornamentation patterns, which are also used occasionally to infer phylogenetic relationships. Scale microornamentation pattern was indistinguishable between the two species and between cervical and midbody scales. The basal (anterior) 400--500 nm end of a scale was characterized by a series of mounds r- 10 pm in diameter. Cells posterior to the mounds were imbricate and brachylamellate, with 1--2 pm long denticles extending from their apical edges. Denticles were longer on cells further from the base. Relatively longer denticles overlapped posterior cell denticles and were organized into distinct linear patterns. Near the apex, shorter denticles no longer overlapped. The similarity in scale microornamentation among species of ratsnakes and related genera suggests either no functional significance, or an unknown common function for species within diverse habitats.

Introduction

The epidermis of squamates is composed of a series of discrete layers, the outermost of which is one cell layer thick and rich in beta keratin (Irish et ah, 1988; Maderson et ah, 1998). This single cell layer, referred to as the Oberhautchen, serves as the interface between the organism and the environment and bears intricate fine sculpturing of the outer surface (Picado, 1931; Irish et ah, 1988). Scale microornamentation has been studied in many species of snakes from diverse lineages (Price, 1982; Stille, 1987; Price and Kelly, 1989; Chiasson et ah, 1989; Gower, 2003). Although used occasionally as a character to help infer phylogenetic relationships (Price, 1982; Stille, 1987; Price and Kelly, 1989; Chiasson et ah, 1989), microornamentation patterns are often similar among species, even those from diverse lineages; consequently, relatively few patterns of microornamentation have been described (Price and Kelly, 1989). For example, scales of many colubrid species have a similar microornamentation pattern: they are lamellate-imbricate at the basal end and echinate at the apical end (Price and Kelly, 1989). Perhaps because of similarity in pattern among several tribes of colubrids, scale microornamentation has been described for relatively few species of lampropeltine snakes (Family Colubridae: Subfamily Colubrinae: Tribe Lampropeltini), and regional variation has not been addressed. Price and Kelly (1989) described microornamentation in four species of lampropeltines: Red Ratsnakes (Pantherophis guttatus), Moellendorffs Ratsnake (Orthriophis moellendorffi), Prairie Kingsnakes (Lampropeltis calligaster), and Milksnakes (Lampro peltis triangulum). Here we examine the fine structure of scales from two species of New World Ratsnakes from middle Tennessee: the Gray Ratsnake, Pantherophis spiloides, and Red Ratsnakes, Pantherophis guttatus.

Materials and Methods

Scales were obtained from specimens previously collected as road-kill in either Cannon or Rutherford counties of Middle Tennessee, fixed in 10% buffered formalin, stored in 70% ethanol, and housed in the MTSU Herpetology collection. We used jeweler forceps to tease the Oberhautchen layer from individual scales located along the mid-dorsal line in the neck (dorsal cervical scales) and in the middle of the body (dorsal midbody scales). We examined scales from two Pantherophis spiloides (n = 20, 12 cervical and 8 midbody) and three Pantherophis guttatus (n = 21, 12 cervical and 9 midbody). These scales were placed in 95% ethanol, air dried, mounted on 15 mm diameter aluminum stubs using spot adhesive, and coated with gold using a Hummer 6.2 sputtering apparatus. We viewed and photographed scales using either a Hitachi S3400N or a Tescan Lyra 3 focused-ion beam scanning electron microscope. Because of variation of microornamentation along the length of a scale, we documented the pattern of microornamentation of the basal, middle, and apical regions of each scale; furthermore, we examined these regions at magnifications between 1000X and 6000X.

Results

Dorsal scale microornamentation was indistinguishable between P. spiloides and P. guttatus, and we detected no difference in microornamentation between scales from the cervical and midbody regions of either species. Dorsal scales exhibited appreciable regional variation from base to apex in relief, cell shape, and microornamentation.

The anterior edge of the basal region of each scale was characterized by a series (several dozen) of mounds or hillocks [less than or equal to] 10 [micro]m diameter (Figs. 1, 2, 3). The mounded region extended 400-500 [micro]m from the basal edge towards the apex. Basal Oberhautchen cells were polygonal and uniformly covered with small pores, 0.3-0.8 [micro]m in diameter (Figs. 2, 3).

The Oberhautchen cells of the microdermatoglyphic transition zone (MTZ) were imbricate and brachylamellate, with echinate apical borders characterized by small (1-2 [micro]m long) spike-like denticles (fimbriae) that lacked pores (Figs. 2, 3). Because the transition in cell shape occurred over a short distance (ca. 100 [micro]m), only the most basally located two to three rows of cells lacked the echinate (fimbriated) border (Figs. 2, 3). The relatively short denticles on the more basally located cells were not organized into any apparent pattern with the denticles from either adjacent posterior or adjacent anterior cells (Figs. 2, 3).

The Oberhautchen cells of the middle and apical region of a scale were imbricate near the MTZ, but became more lamellate apically (thinner basally to apically and wider from side to side) (Fig. 4). The denticles (fimbriae) forming the echinate border were increasingly longer on cells further from the base and closer to the apex, with denticles from cells in the middle region of a scale exceeding lengths of 10 [micro]m (Fig. 5). In contrast to more anterior cells with relatively short denticles, cells in the middle of a scale had relatively long denticles that were organized with denticles from adjacent posterior and anterior cells into distinct patterns. These patterns became apparent in cells with denticles that were longer than the cells were wide (Fig. 5). In these cells, specific denticles were overly elongated compared to adjacent denticles. The elongated denticles coincided with comparably elongated denticles of adjacent anterior and posterior cells, such that a series of elongated denticles formed distinct, albeit tiny, lengthwise ridges (Fig. 5). Thus, beyond the basal area, which was overlain by an adjacent anterior scale, the gross, superficial smooth or glossy appearance of dorsal scales disguised a series of fine striations or ridges formed from organized elongated denticles (Fig. 6). Indeed, this organization formed a series of thin channels between rows of overlain denticles that extended to near the most posterior (apical) edge of the scale (Fig. 7).

Bacteria were found on several of the scales examined, regardless of the location that the scales were removed from the body. Often bacteria were isolated, but occasionally the bacteria were found in relatively dense clusters (Fig. 8).

Discussion

We could not distinguish microornamentation of dorsal scales between Pantherophis spiloides and P. guttatus, and our observations on the latter species are similar to those of Price and Kelly (1989) who also reported that the dorsal scales in P. guttatus are lamellate and imbricate in the basal region, and are echinate in more apical regions. Scale ornamentation has been characterized for other species of the colubrid tribe Lampropeltini, including Prairie Kingsnakes (L. calligaster) and Milksnakes (L. triangidum) (Price and Kelly, 1989); microornamentation in these species is, apparently, similar to that of Pantherophis species.

The habitat preferences of the Lampropeltini are diverse, including species often found in trees (P. spiloides, P. guttatus) and species that largely are fossorial (Lampropeltis calligaster). Nonetheless, scale microornamentation is essentially indistinguishable among these species (Price and Kelly, 1989), suggesting either no functional significance associated with dorsal scale microornamentation in species of this tribe, or a common function of the microornamentation among species in diverse habitats. Regardless, the similarity of microornamentation in the lampropeltines in general and in Pantherophis specifically stands in stark contrast to the variation in microornamentation reported among congenerics and closely related genera from other colubrid tribes, or within other families of snakes (e.g., Agkistrodon, Chiasson et ah, 1989; Crotalus and Sistrurus, Stille, 1987; Nerodia, Thamnophis, Chiasson and Lowe, 1989). Although apparently useful as a taxonomic character in some genera (Hoge and Santos, 1953; Dowling et al. 1972), we suggest that microornamentation is not a useful taxonomic character in species of Pantherophis.

Various functions have been attributed to several of the microornamentation patterns documented in snakes, including shedding or trapping of dirt (Gans and Baic, 1977; Gower, 2003), production of iridescence (Gower, 2003), adjustment of friction to facilitate locomotion (Berthe et ah, 2009; Rocha-Barbosa and Moraes e Silva, 2009), and retention or spread of pheromones or oils between molts (Smith et ah, 1982). McCarthy (1987) proposed that the relatively simple scale microornamentation in sea snakes (Laticauda colubrina: brachylamellate basally, cellular polygonal imbricate apically; McCarthy 1987, Price and Kelly, 1989) when compared to the relatively more complex microornamentation of terrestrial elapids was "perhaps connected with an anti-fouling strategy". The lamellate imbricate basal and echinate apical scale microornamentation pattern of Pantherophis guttatus, P. spiloides, and other lampropeltine snakes is a common pattern found among diverse lineages of snakes (Price and Kelly, 1989). Nonetheless, functional attributes of this common pattern are speculative and await experimental analyses (e.g., bacterial shedding, dirt shedding, etc.) However, if microornamentation affects the shedding of dirt (Gower, 2003), perhaps it also affects shedding of bacteria and fungal spores.

To our knowledge, no one has compared the extent of bacterial colonies on scales among species of snakes exhibiting different patterns of microornamentation. That we found bacteria on many of the scales we examined is not surprising; all our scales were obtained from specimens collected as roadkills. Furthermore, we did not attempt to quantify bacterial colonies and we are not aware if bacteria loads vary among different species of snakes, or among snakes with different microornamentation patterns. Perhaps the recent concern about fungal skin infections in snakes (Allender et ah, 2011) will renew interest in scale microornamentation and studies will be conducted that examine the possible effectiveness of different patterns as antibacterial surfaces (sensu lato Hasan et ah, 2013).

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Received 16 December 2014; accepted 1 April 2015.

Brian T. Miller *, Abby Drumwright, Herschell Parker, and Joyce L. Miller

Department of Biology, Middle Tennessee State University, Murfreesboro, TN 37132 (BTM, AD, HP) MTSU Interdisciplinary Microanalysis and Imaging Center, Middle Tennessee State University, Murfreesboro, TN, USA (JLM)

* Corresponding Author
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Author:Miller, Brian T.; Drumwright, Abby; Parker, Herschell; Miller, Joyce L.
Publication:Journal of the Tennessee Academy of Science
Article Type:Report
Date:May 1, 2015
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