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Histology of the Skin of Three Limbless Squamates Dwelling in Mesic and Arid Environments

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Histology of the Skin of Three Limbless Squamates Dwelling in Mesic and Arid Environments THE ANATOMICAL RECORD 299:979–989 (2016) Histology of the Skin of Three Limbless Squamates Dwelling in Mesic and Arid Environments 1,2 3 1 AHMED A. ALLAM, * JUAN D. DAZA, AND RASHA E. ABO-ELENEEN 1Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef 65211, Egypt 2College of Science, Zoology Department, King Saud University, Riyadh 11451, Saudi Arabia 3Department of Biological Sciences, Sam Houston State University, Huntsville, Texas ABSTRACT The skin of limbless squamates has an increased contact with the substrate compared with limbed counterparts. Comparatively, the contact with the substrate is intensified in fossorial species, where the whole cir- cumference of the body interacts with the soil during underground loco- motion. Although fossoriality in Squamata, specifically lizards and snakes, has been studied ecologically and morphologically (e.g., osteologi- cal changes), not enough detail is yet available regarding changes in organs critical for underground lifestyle such as the skin. Here we used histological and microscopical techniques (scanning electron microscopy and transmission electron microscopy) to uncover the structural detail of the epidermis and dermis in three limbless reptiles, the amphisbaenian Diplometopon zarudnyi, and two snakes, Indotyphlops braminus (Typhlo- pidae) and Cerastes cerastes (Viperidae). The skin of these taxa shows pronounced morphological diversity, which is likely associated to different environmental and functional demands upon these reptiles. Anat Rec, 299:979–989, 2016. VC 2016 Wiley Periodicals, Inc. Key words: dermis; epidermis; Diplometopon zarudnyi; Indoty- phlops braminus; Cerastes cerastes; amphisbaena; serpentes Living non-avian reptiles include a very heterogene- the scale morphology of squamates dwelling in different ous vertebrate assemblage, as well as being one of the environments have proposed that animals inhabiting most species rich class of land vertebrates, surpassing warm-dry and warm areas have larger scales in smaller 10,200 described taxa today (Daza, 2014; Uetz, 2015). Reptiles are the most abundant vertebrates in deserts, where they occupy almost every conceivable habitat Grant sponsors: King Saud University; Deanship of Scientific available (Pianka, 1986, 1989). Diversification of lizards Research; College of Science Research Center; Department of is high in arid tropical and subtropical regions world- Biological Sciences; the Office of the Dean of the College of Sci- wide, except in South America—Atacama and Patago- ence; Office of Research and Sponsored Programs at Sam Hous- nian deserts, while snakes are more abundant in forests ton State University. of tropical latitudes, and extend into temperate latitudes *Correspondence to: Ahmed A. Allam, Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef 65211, north and south of the equator (Ditmars, 1931; Pianka Egypt. Fax: 12-082-2334551. E-mail: [email protected] and Vitt, 2003, Pincheira-Donoso et al., 2013). and [email protected] There is a frequent misconception about the scaled Received 27 January 2015; Revised 5 March 2016; Accepted 8 integument of reptiles, which is commonly referred as March 2016. an adaptive trait for water retention that allows for rep- DOI 10.1002/ar.23356 tiles to flourish and adapt to a terrestrial life (e.g., Published online 25 April 2016 in Wiley Online Library Pough et al., 2013). Morphological studies considering (wileyonlinelibrary.com). VC 2016 WILEY PERIODICALS, INC. 980 ALLAM ET AL. numbers than those dwelling in colder regions (Calsbeek Boyde, 1974; Abo-Eleneen and Allam, 2011). The superfi- et al., 2006; Wegener et al., 2014; Tulli and Robles, cial dermis is always relatively loosely packed with a 2015), supporting the hypothesis that larger scales per- much denser-packed deep dermis. The latter is attached form better as a heat exchanger and water conservation to the muscle fascia by subcutaneous connective tissue structure in arid environments. In contrast, it has been (or hypodermis), the amount of which varies among body argued that the integument of some reptiles is a signifi- regions and species. In addition to fat cells, nerve axons, cant path for evaporative water loss, which even exceeds and blood vessels, the dermal matrix provides two cell respiratory water loss (See revision in Lillywhite and types of particular significance in reptiles: the chromato- Maderson, 1982). Consequently, reptile scales alone do phores and the scleroblasts. Chromatophores are promi- not provide waterproofing; this quality is determined nent in anamniotes and lepidosaurians, where they form also by lipids, which provide an effective water barrier dermal chromatophore units that are responsible for both (Landmann, 1986; Lillywhite, 2006; Miller and Lut- permanent and transient coloration patterns (Bagnara terschmidtt, 2014; Pough et al., 2016). Recently it has et al., 1979). Chromatophores have been shown to derive been found that some snakes also bear a microscopic from the neural crest (Noden, 1980). Pigment cells have lipid coating on both dorsal and ventral scales that func- also been identified in the dermal skin of reptiles tion as a lubricant and prevent scale wearing especially (Bagnara, 1998). Scleroblasts form a dermal skeleton in on the ventral surface (Baio et al., 2015). This conclusion many different vertebrates and may also originate from is reinforced by empirical data derived from experimen- the neural crest (Hall, 1980). tal observations of one scaleless and one typical snake Interactions of skin with the soil surface, such as fric- with scales, where no difference in water loss was tional resistance and adhesive properties affect the rep- observed between individuals of comparable age and size tile’s outer skin surface especially in limbless and (Licht and Bennett, 1972). Physiological studies on liz- strictly fossorial animals such as the majority of amphis- ards and snakes concluded that lipid content in the baenians (Gans, 1960). Dietary preference for large prey integument and differences in scale morphology are two also can have some effect on the skin—the observable nonmutually exclusive mechanisms by which organisms distensibility of snake skin facilitates accommodating from arid environments can limit rates of water loss and swallowing large food items (Gans, 1974). Likewise, (Gunderson et al., 2011). morphological traits such as high numbers of scale rows In squamates, the ultrastructure of the skin might in the skin in snakes might assist distension during play an important physiological function for water bal- swallowing (Pough and Groves, 1983). ance and protection. Early attempts to reveal the under- In reptiles, the majority of scales are characterized by lying anatomy of the skin in reptiles dates back to the an expanded outer surface, a short inner surface, and a 1800s (Dumeril et al., 1834), and although there are hinge region (Landmann, 1986). Scales also vary and dif- some modern studies that have elaborated with better fer according to the location in the body region (Mader- optical devices and provide a generalized idea of the son et al., 1998), or according to environmental impact integument on squamates (e.g., Maderson, 1965; Gans, (Allam and Abo-Eleneen, 2012). In snakes the scaled 1974; Alibardi and Toni, 2006; Abo-Eleneen and Allam, skin is formed by two regions that contrast drastically in 2011), more anatomical detail is required to understand histology, a region formed by a series of elevated, thick- the effect of the environment on the cellular structure of ened horny epidermal scales and another region formed the skin. by thin inter-scale hinge regions (Maderson, 1965; Gans, In squamates, the epidermis is characterized by an 1974; Alibardi and Toni, 2006; Abo-Eleneen and Allam, alternating vertical distribution of keratin types, the 2011). Anatomical details on the epidermal scales of superficial part consists of cornified epidermis made of snakes have been studied, such as the carbohydrate his- b-type keratin, while the underlying part is made of a- tochemical distribution (Natrix tessellata and Cerastes type keratin (Lillywhite and Maderson, 1982). The cor- vipera; Abo-Eleneen and Allam, 2011), mucous cells in neous b-proteins layers are thick on the outer surface the epidermal hinge region and carbohydrate distribu- and are represented by only one cell layer (Ober- tions in the epidermal cells (Xenochrophis piscator, hautchen)€ in the hinge region. Conversely, the a-keratin Banerjee and Mittal, 1978). layer is fairly uniform in thickness over the entire body In this study we reviewed the histology of three limb- surface. This distribution of protein types can be less, burrower squamates with different microhabitats in explained as follows: the outer scale surface which is Saudi Arabia and Egypt—the introduced Indotyphlops exposed to mechanical stress is strengthened by the stiff, braminus (Fig. 1A, Typhlopidae) which burrows on resistant corneous b-proteins (Spearman, 1969; Alibardi, mesic soils, Diplometopon zarudnyi (Fig. 1B, Trogono- 2015), while the areas of the hinge regions, which facili- phiidae), and Cerastes cerastes (Fig. 1C, Viperidae) tate movement of the body regions relative to each other, which burrow or dwell in dry and/or shifting sand envi- are covered by the elastic and pliable a-type keratin ronments (Said-Aliev, 1963). We focused on determining (Spearman and Riley, 1969). Because of rectilinear loco- adaptations to microhabitat selection of the surface and
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