Comparative Morphology of the Skin of Natrix Tessellata (Family: Colubridae) and Cerastes Vipera (Family: Viperidae) Author(S): Rasha E
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Comparative Morphology of the Skin of Natrix tessellata (Family: Colubridae) and Cerastes vipera (Family: Viperidae) Author(s): Rasha E. Abo-Eleneen and Ahmed A. Allam Source: Zoological Science, 28(10):743-748. Published By: Zoological Society of Japan DOI: http://dx.doi.org/10.2108/zsj.28.743 URL: http://www.bioone.org/doi/full/10.2108/zsj.28.743 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ZOOLOGICAL SCIENCE 28: 743–748 (2011) ¤ 2011 Zoological Society of Japan Comparative Morphology of the Skin of Natrix tessellata (Family: Colubridae) and Cerastes vipera (Family: Viperidae) Rasha E. Abo-Eleneen1 and Ahmed A. Allam1,2* 1Department of Zoology, Faculty of Science, Beni-suef University, Beni-Suef 65211, Egypt 2King Saud University, College of Science, Zoology Department, Riyadh 11345, Saudi Arabia We studied beneficial difference of the skin of two snakes. Two snakes were chosen from two dif- ferent habitats and two families: Colubridae (Natrix tessellata) and Viperidae (Cerastes vipera). The investigations were performed by light and electron microscopy. Histologically, the skin of the stud- ied species show pronounced modifications that correlated with functional demands. The scales in Natrix tessellata overlapped slightly, while in Cerastes vipera they were highly overlapped. SEM shows that scales of Natrix tessellata had bidentate tips while the scales of Cerastes vipera were keeled. Histochemically, in both studied species, melanocytes and collagenous fibres were distrib- uted throughout the dermis. Polysaccharides were highly concentrated in the epidermis and dermis of both species while proteins were highly concentrated only in the epidermis. Transmission elec- tron microscopy (TEM) showed that the skin of both snakes consisted of keratins located in the epidermis. Some lipids and mucus were incorporated into the outer scale surfaces such that lipids were part of the fully keratinised hard layer of the snakes’ skins. Lipids are probably responsible for limiting water loss and ion movements across the skin. Melanosomes from epidermal melano- cytes were present only in Cerastes vipera. In aggregate, these results indicate that snakeskin may provide an ecological indicator whereby epidermal and integumentary specializations may be eco- logically correlated. Key words: snake, skin, reptiles, histochemistry, scales The epidermis of reptiles produces two classes of INTRODUCTION keratins: soft, or alpha-keratins, and hard, or beta-keratins Reptiles are terrestrial animals that have become com- (O’Guin et al., 1987; Alibardi and Toni, 2006). The epidermis pletely independent of the aquatic environment; their skin is of Natrix piscator is complex in its organization and consists dry and has low permeability to water. All reptilian species of a series of small discrete units, with the scales contiguous have characteristically scaly skin, which is one of the main at the hinge region (Singh, 1989). Goslar (1958), in describ- features distinguishing them from other amniotes (birds and ing the scale epidermis of Natrix natrix, gave a concise mammals). The reptilian integument protects the animal account of the carbohydrate histochemistry. Baberjee and from mechanical damage and dehydration (Maderson et al., Mittal (1978) reported mucous cells in the hinge epidermis, 1985; Matoltsy and Bereiter-Hahn, 1986). The different and described carbohydrates in cellular components of the scale patterns observed are a result of a long evolutionary epidermis of Natrix piscator. The first comparative micro- process that allowed each species to adapt to its specific scopic study of vertebrate integumentary development environment (Alibardi and Toni, 2006). included observations on embryos of Natrix sp., Anguis The epidermis is derived from the embryonic ectoderm, fragilis and Lacerta sp. (Kerbert, 1876), and described the while the dermis is derived from somatic mesoderm. The two-layered condition of the epidermis in early stages of rep- dermis may be closely or loosely attached to the fascia of tiles and birds. The report argued that this condition was deeper muscles (Hall, 1980; Noden, 1980). Both the epi- common to all vertebrates, quoting observations on fish dermis and the dermis may contain neural crest-derived pig- (Rienecke, 1869) and amphibians (Stricker, 1872). ment cells, although those seen in the epidermis are usually A scaled integument with dermal ossification was pres- only of the melanogenic type (Noden, 1980). ent in basic amniotes of the Carboniferous Period, which were by definition reptiles, about 340 million years ago * Corresponding author. Phone: +2-012-2928210; (Colbert et al., 2001; Pough et al., 2001). Skin morpho- Fax : +2-082-2328088; genesis and epidermal differentiation in therapsids and sau- E-mail: [email protected] ropsids probably began to diversify since the Upper Carbon- doi:10.2108/zsj.28.743 iferous, as suggested by anatomical and paleontological 744 R. E. Abo-Eleneen and A. A. Allam data (Maderson and Alibardi, 2000). Integument evolu- tion in reptiles was centred on variations of scale shape in relation to adaptation to their habitat, functional pur- poses (especially water-loss limitation), composition, and degree of keratinization (Sawyer and Knapp, 2003; Saw- yer et al., 2003; Wu et al., 2004). Scales protect the body of the snake, aid it in loco- motion, and allow moisture to be retained (Gans, 1974; Mullin, 1996). Broad variations of scale morphology, size, and overlap is found in modern reptiles, repre- sented by the numerous species of lizards and snakes (Pough et al., 2001). These variations include the numer- ous variations in their superficial micro-ornamentation (Arnold, 2002). The present study is concerned with the histochem- ical characterization of carbohydrates, proteins in the scales, hinge epidermis of a water snake and a sandy snake as well as with the difference in the skin of two selected snakes. The first was Natrix tessellata, which is one of the most common snakes in the vicinity of the Nile Area (water) in Egypt. Its maximum length is 1.0–1.3 m. The colour may vary from greyish green to brownish or almost black, with dark spots on the back (Vlcek et al., 2010). The second was Cerastes vipera, which is small and stout having an average length of 35–55 cm. It has a broad, triangular head with small eyes set well forward and situated on the junction of the side and the top of the head. It is a sandy desert species (Mallow et al., 2003). MATERIALS AND METHODS In the present study, 20 specimens of Natrix tessellata (Hanas El Maiya) were captured from the Egyptian Nile Delta regions (water habitats), and 20 specimens of Cerastes vipera (Haiya Qarah) were collected from sandy areas in the Mediterranean coastal desert of Egypt. Histological assay The skin of the specimens were directly fixed in 10% neu- tral formalin, then washed and dehydrated in ascending grades of ethyl alcohol, cleared in xylene, and embedded in paraffin. Serial 5 μm sections were cut and stained with Ehrlich’s haema- toxylin and eosin (Mallory, 1944). Periodic acid/Schiff’s (PAS) Fig. 1. (A–J) Light micrograph of vertical sections through skin. (A) Skin of method was used for polysaccharide staining (McManus, 1946). Natrix tessellata showing the slight overlapping scales separated by hinge In PAS, an acetylation blocks the hydroxyl groups from forming regions (H). Outer (OSS) and inner (ISS) scale surfaces are clearly differenti- acetyl esters, and a deacetylation hydrolyzes the acetyl esters ated (H.E., X 100). (B) Higher magnification of (A) showing that epidermis (E) and unblocks the reactive hydroxyl groups. To differentiate neu- and dermis (De) are clearly distinct. Melanocytes (M) and collagenous fibres tral mucopolysaccharides from the acid mucopolysaccharides, (Cf) are present in the dermis (H.E., X 400). (C) Skin of Cerastes vipera PAS/AB staining (Mowry, 1956) was employed. Bromophenol showing the high overlapping scales. The scales are separated by hinge blue was used for staining proteins (Mazia et al., 1953) to show regions (H) (H.E., X 100). (D) Higher magnification of (C) showing the epider- hardness. These sections were examined and photographed mis (E), dermis (De), collagenous fibres (Cf) and rare melanocytes (M) in the dermis (H.E., X 400) (E) Skin of Natrix tessellata showing accumulation of using a Leitz microscope. PAS positive material in the epidermis (E), the dermis (De) and the muscles (Mu) (PAS., X 100). (F) Skin of Cerastes vipera showing large amounts of Scanning electron microscopy (SEM) PAS positive material in the epidermis (E) and the dermis (De), the muscles Natrix tessellata and Cerastes