Ecological aspects of the horned viper, Cerastes cerastes gasperettii in the central region of Saudi Arabia.

Feeding ecology of any species can help us to understand its natural history, ecological requirements and approaches involved in searching for food. Feeding ecology and sexual dimorphism in the horned viper, Cerastes cerastes gasperetti collected from the Al-Thumama area, central region of Saudi Arabia was described. The gut content of Cerastes c. gasperetti mainly consisted of rodents (70%) in addition to arthropods (15%) and lizards (10%). Least sexual size dimorphism was noticed in the species in terms of total length. Significant difference was noticed between males and females in terms of two correlation points vent tail length (VT) and total length (TL) with the males attaining a larger size (P < 0.05). The mean number of the dorsal body scales, ventrals and subcaudals for the females was 102, 156 and 33 scales respectively which were significantly different from respective ones in males 95, 160 and 38 scales. There are many aspects of the feeding of this snake that remain unknown and further studies are clearly needed.

Introduction

Snakes are considered to be exceptional model organisms (Shine and Bonnet, 2000), in part because of their unique adaptations for feeding and foraging (Greene, 1997). Limited ecological studies have been done on snakes and lizards of different geographical regions of Saudi Arabia viz., Southern Hijaz (Parker, 1938), Eastern Arabia and Northeastern Arabia (Mandaville, 1967), Central Arabia (Al-Wailly and Al-Uthman, 1971), and Riyadh (Al-Sadoon and Al-Otaibi, 2014). Studies of diet can provide valuable insights into the biology of snakes, including their evolutionary divergence (Colston et al., 2010), movements and habitat use (Heard et al., 2004, Lillywhite et al., 2008, Baxley and Qualls, 2009), interspecific competition and community structure (Nowak et al., 2008), and conservation (Holycross et al., 2002b). Although some snakes are specialists with narrow diets, many exhibit a substantial variation in diet at both individual and population levels (Greene, 1997). Understanding geographic variation in diet can benefit our knowledge of venom composition (Barlow et al., 2009); the relationships between environment, body size, and sexual size dimorphism (Amarello et al., 2010); and, potentially, trophic morphology (Vincent et al., 2009).

External morphology of an organism is the outcome of the interaction between the organism itself and the habitat in which it lives (Greene, 1997). Most snake species exhibit sexual dimorphism in body size, with females larger than males (Fitch, 1981). Sexual head size dimorphism has also been documented in rattlesnakes (Glaudas et al., 2008), and may be associated with sexual differences in diet (Vincent et al., 2004).

Body size and various other external characteristics have an impact on the life of an organism, acting on its capacity to adopt itself to face the situations in order to survive, grow up and reproduce (Fornasiero et al., 2007). Sexual size dimorphism in different viper, elapid, and colubrid species has been reported for snout–vent length, relative head size, head shape, relative tail size, and mass (Krause et al., 2003). Another sexual difference among snake species is that males have longer tails than females (Rossman et al., 1996). Due to their relatively simple structure and organization, snakes check variations in morphological and morphometrical features caused by different ecological pressures. Besides, variations in body size and relative body mass have been specifically correlated to the abundance and availability of prey (Schwaner and Sarre, 1988).

The horned viper Cerastes cerastes gasperetti (Gasperetti’s sand viper) belongs to the family Viperidae which is the most common snake in Saudi Arabia (Al-Sadoon et al., 2013). However, this snake has received little interest, even though it is distributed throughout many deserts, mostly in Egypt, Jordan and Saudi Arabia (Al-Sadoon, 1989). Horned viper is a nocturnal true desert snake and prefers sandy soil with some vegetation as shelters. Horned vipers, which comprise one of the most-studied groups of snakes, are generally recognized as opportunistic predators with varied diets; yet no study has specifically addressed the diet of the species, Cerastes c. gasperettii. Therefore, the study of an organism’s feeding habits and its external morphology may be a valuable approach to understand the ecological aspects of this species.

Materials and methods

A total of 238 specimens (males, n = 115; females, n = 123) of the horned viper, Cerastes c. gasperettii were collected from Al-Thumama area, in the central region of Saudi Arabia for a period of one year from May, 1998–April, 1999. Ecological field studies including morphological characters and the mode of nutrition were carried out. The captured snakes were transported to the Reptilian Laboratory in the Zoology Department, College of Science, King Saud University where all experimental procedures were performed. Animals were kept at ambient temperature and with natural photoperiod.

Standard morphological measures of all specimens were taken and the parameters studied were: snout–vent length (SV), vent tail length (VT) and total length (TL), number of dorsal scales (DS) according to Gasperetti (1988), number of ventral scales (VS) and number of subcaudal scales (SCS).

The animals (n = 80) were killed by freezing at −2 °C for 24 h. A mid-ventral incision was made to determine presence/absence of food items in stomach contents and fecal matter. Prey items and stomach, gut, and fecal contents were stored individually in sealed glass vials containing 70% ethanol. Prey items were classified as arthropods, lizards, rodents, or unknown.

The experiments were conducted in agreement with the standards mentioned in the guidelines for the care and use of experimental animals by the King Saud University, Riyadh, Kingdom of Saudi Arabia.

Results

Through the study of 238 samples of this species, results showed that Cerastes c. gasperettii are similar to Cerastes cerastes, but the head is slightly wider and flat and the scales of the upper lip are small and there are no swollen warts on the occipital region. There is a pair of scale like horns above the eyes. But these horns are oblique to the dorsal side and not dorsally vertical as in Cerastes cerastes. The head color of Cerastes c. gasperettii is different than Cerastes cerastes, where the dark diagonal line behind the eyes is thin and relatively longer. The shaded areas on the dorsal site have a parallel weak and faint line, and contain a series of dotted rhombic shapes. Cerastes c. gasperettii showed a camouflage character e.g. they become red on sandy soils and gray in desert plains.

In terms of snout–vent length (SV) no significant difference was observed between males and females with the males attaining a slightly longer size than females (P > 0.05). Significant difference was noticed between males and females in terms of two correlation points VT and TL (r = 0.9998) with the males attaining a larger size (P < 0.05). Vent-tail length showed significant differences (P < 0.05) as adult males (VT = 62 mm) were longer than females (VT = 49 mm). In case of males VT (62 mm) comprised a significantly larger part of TL (552 mm). However, VT comprised (49 mm) of the TL (538 mm) in females (Fig. 1).

Figure 1

Length measurements for Cerates c. gasperettii.

For females the mean number of the dorsal body scales, ventral body scales and subcaudal scales was 102, 156 and 33 scales, respectively, which was significantly different from respective ones in males 95, 160 and 38 scales (Fig. 2). The three correlation points of the dorsal scales anterior (34), mid body (35) and posterior (33) were significantly higher in females than the males (r = 0.9984). Table 1 displays the comparison between the results obtained from this study and the results of Werner et al. (1991).

Figure 2

Number of scales for Cerates c. gasperettii.

Table 1

Comparison between the results obtained from this study and the results of Werner et al. (1991).

Scale types	Sex	n	Measurements recorded		Measurements Werner et al. (1991)
Range	x¯	n	Range
VS	Male	115	138–167	160	59	146–159
Female	123	144–165	156	92	152–167
DS	Male	115	24–35	32	56	22–41
Female	123	26–36	34	92	22–38
SCS	Male	115	29–44	34	31	30–35
Female	123	15–46	33	61	30–37

Eighty specimens both males and females of the Cerastes c. gasperettii were studied for gut content analysis. The result of stomach contents indicates that Cerastes c. gasperettii is carnivorous. It feeds mainly on Rodents (Gerbillus cheesmani and Mus musculus) which were found in snakes with a larger size and formed 70% of the stomach contents. Arthropods (beetles) constituting 15% of the content and lizards (Acanthodactylus schmiditi and Stenodactylus slevinii) form 10% of the total diet. The remaining 5% of the stomach content was completely digested and could not be identified (Fig. 3).

Figure 3

Stomach contents of the Cerastes c. gasperettii.

Discussion

Regarding the geographical distribution of Cerastes c. gasperettii in the central region of Saudi Arabia, it has been observed that it is scattered all around sandy areas of Saudi Arabia. Our data confirmed that adult Cerastes c. gasperettii males averaged slightly larger in body length than females. Snout–vent length was not markedly dimorphic in this species. Although most snake species exhibit female-larger sexual size dimorphism (Shine, 1991), females averaged larger in body length than males in Eryx jayakari (Al-Sadoon and Al-Otaibi, 2014). Other than body size, the meristic parameters were not highly dimorphic, with males showing a higher number of ventral scales than females.

Documenting the diet and foraging behavior of a snake species is often the first step in the development of an understanding of its ecology (Rodriguez-robles et al., 1999). A detailed description of the food habits of a predator can enable subsequent users of these observations to place them in a broader ecological and evolutionary context (Green, 1993). Dietary information can be used, for example, to evaluate hypotheses about biological diversification, to predict aspects of ecology of closely related taxa, or guide conservation efforts (Green, 1994).

Analysis of the stomach content of the Cerastes c. gasperettii showed that the preferred food is primarily rodents throughout the year, followed by Arthropods and Lizards. Our data revealed that Cerastes c. gasperettii specializes on mammalian prey (70% of all prey items), supporting the general consensus of anecdotal reports found in the literature (Campbell and Lamar, 2004). Terrestrial rodents constituted the primary prey source. Rodents (G. cheesmani and M. musculus) were the most abundant prey species (70%). Comparable reliance on a mammalian prey base has been reported for the rattlesnake species, including Crotalus atrox (>80%; Reynolds and Scott, 1982) and Crotalus catalinensis (70.7%; Avila-Villegas et al., 2007). Al-Sadoon and Al-Otaibi (2014) reported 25% of rodents in the stomach contents of Sand Boa, E. jayakari. The preference to the rodents may be due to their nocturnal activity and the abundance of these organisms.

Arthropods compose 15% of the total prey items and are found in the gut content of Cerastes c. gasperettii whereas Arthropods (beetles) constitute 12.5% of the content in E. jayakari (Al-Sadoon and Al-Otaibi, 2014). Lizards represent only a small portion of the diet (10%) and are occasionally taken by Cerastes c. gasperettii. Thus, Cerastes c. gasperettii consumes primarily rodents at different stages of life, as stated earlier for Crotalus durissus (da Graça Salomão et al., 1995) whereas the lizards constitute 50% of diet in Sand Boa, E. jayakari (Al-Sadoon and Al-Otaibi, 2014).

Small birds, lizards and amphibians are considered as the main food for Bitis arietans (Broadley, 1983), while small rodents, lizards and small birds are considered as the main food for Cerastes gasperettii (Gasperetti, 1988). Larger animals tend to feed upon larger prey, hence leading to decreased interspecific and intraspecific competition (Best and Gennaro, 1984). However, seasonal, habitat, phylogenetic, and other influences may contribute to or override the effects of body size on dietary tendencies.

Even though vipers comprise one of the most-studied groups of snakes, detailed studies of many ecological aspects are still lacking for the majority of species. Cerastes c. gasperettii, is dimorphic in both size and shape except snout–vent length, with males attaining a larger size than females. Single-species studies enhance an upward comparative literature on snake feeding ecology and sexual dimorphism that can be used to test hypotheses on the evolution of diet and associated adaptations for procuring food.