The South-American rattlesnake Crotalus durissus : feeding ecology in the central region of Brazil

We investigated food patterns in the diet composition of 452 specimens of Crotalus durissus from Central Brazil. Thirty-three items were recorded corresponding to four categories: rodents (75.76%), marsupials (6.06%), unidentified mammals (9.09%) and reptiles (9.09%). Adults of both sexes and some juveniles feed mostly on mammals, specifically rodents, it is the most active and abundant prey throughout the year mainly in areas from Cerrado. In addition, we observed that in C. durissus there is a trend in the diet of females could be more diverse, maybe this can be associated to sexual differences involving different strategies of the feeding biology of this rattlesnake.


Introduction
The rattlesnakes of the genus Crotalus evolved in North America and subsequently spread across Central and South America (Echevarrigaray et al. 2000;Quijada-Mascareñas et al. 2007).Currently 41 species of Crotalus are recognized, with greater a diversity in Mexico and the United States (Uetz at al. 2016).This genus is frequently considered as a model for studies related to ecology, due to its widespread distribution covering several habitats, including deserts, flooded areas, forest environments and open habitats (Norman, 1994;Beaupre et al.1998;Place & Abramson, 2004).
In many species of Crotalus there is ontogenetic variation in diet, with juveniles feeding primarily on ectothermic prey whereas adults prefer endothermic animals as food.Moreover, there is extensive inter-and intraspecific variation in the diet of rattlesnakes.The smaller species, feed primarily on arthropods, amphibians and lizards whereas larger species feed on lizards and small mammals (Klauber 1956(Klauber , 1972)).For instance, adult Crotalus horridus from several regions of the United States (Clark 2002) as well as C. viridis in southeast Idaho (Diller & Wallace 1996) feed mainly on birds and small mammals.Crotalus vegandris from Venezuela (Pífano & Rodriguez-Acosta 1996), C. pricei, and C. lepidus from some areas in Mexico and the United States (Holycross et al. 2002;Prival et al. 2002), feed on centipedes, lizards, and snakes.However, a divergence in the diet composition was detected in two populations of C. lepidus at Big Bend National Park, Texas (Beaupre 1995).In a similar way, the diet of C. viridis oreganus from California is more diverse when compared to C. viridis from British Columbia, mainly because of the greater importance of ectothermic prey (Macartney 1989).
The South-American Rattlesnake Crotalus durissus, is restricted to South America (Campbell & Lamar 2004) and has a discontinuous distribution (Wüster et al. 2005) from Colombia to Argentina (Vanzolini et al. 1980).Some populations exhibit considerable ecological variation, with closeby populations differing greatly from each other (Campbell & Lamar, 2004).
In Brazil, Crotalus durissus is widely distributed, except for the states of Acre and Espírito Santo.In addition, there are isolated populations in open areas within savannas of the Amazonian Forest (Campbell & Lamar 1989).The diet of the species is assumed to be characterized by an extreme specialization in endothermic prey; a feature that exists for only a few species of rattlesnake and which is thought to represent an ancestral trait (Clark 2002).Studies of food composition in populations from southeastern Brazil indicated that rodents and small marsupials were the prey more widely eaten by rattlesnakes (Sant'Anna & Abe 2007); however, birds (Vanzolini et al. 1980) and lizards (Santos & Germano 1996), can be considered as occasional food items in the C. durissus diet.In this work, we describe the feeding ecology of Crotalus durissus in the central region of Brazil and discus some strategies involved in the feeding of this rattlesnake.

Material and Methods
The snakes examined represent a total of 452 individuals of Crotalus durissus from the central region of Brazil covering forest formations of the Amazon and Atlantic forests, Caatinga and Cerrado; identified as 213 males, 167 females and 72 neonates and juveniles.We considered specimens to be neonates when their snout-vent length was smaller than 400mm (Hoyos, 2012).The specimens are housed in the scientific collections of Instituto Butantan (IBSP), Museu de Zoologia da Universidade de São Paulo (MZUSP), and Universidade de Brasília (CHUNB).Animals kept in captivity prior to being deposited in a scientific collection were excluded from this study.
All food items were removed from the stomach and identified to the lowest possible taxonomic level.Each of the contents was deposited in a glass container with the same identification number as the specimen (voucher number).The intestinal content was determined while taking into account the type of food residue.In addition, available literature records of prey were included in this study, which analyzed the food composition for Crotalus durissus from southeastern Brazil (Santos & Germano 1996;Sant'Anna & Abe 2007).

Results
Thirty-three items were recorded in 30 (7%) stomachs.Approximately 52 (12%) of the intestines contained hair.Four prey categories were identified in the stomachs, the main being rodents 75.76% (Figure 2), marsupials 6.06%, followed by unidentified mammals 9.09% and reptiles 9.09% (Figure 3).The rodents were registered in almost all forest formations studied; marsupials were registered only in Cerrado sites, and lizards in areas of Caatinga and Cerrado (Figure 1) (Appendix 1).In addition, these results show a slight trend towards increased consumption of lizards in females.Evidence for ontogenetic or sexual variation was not detected (Table 1).
Overall, the diet composition of the South-American Rattlesnake Crotalus durissus, considering information of stomach contents identified from specimens in this study in combination with literature records (Santos & Germano 1996;Sant'Anna & Abe 2007), show a similar feeding patterns: rodents 66.05%, marsupials 3.98%, unidentified mammals 28.38% and reptiles 1.59%; in reference to the reptiles, only six specimens -four of which identified in females had reptiles in their stomach.

Discussion
Considering data to other viperids (Sawaya et al. 2008;Marques et al. 2009;Barbo et al. 2011) the frequency of individuals of Crotalus durissus with prey in the stomach was low.
The elapsed time between capture of the snake and its preservation probably is a reason for the low number of prey in the stomach.This is also supported by Sant'Anna & Abe 2007, where the stomach content of C. durissus from southeaster Brazil showed a much lower proportion than the gut content.
Approximately 90 percent of rattlesnakes of the genus Crotalus, exhibit ontogenetic shifts in food composition, changing from ectothermic to endothermic preys.These variations could be attributed to changes in morphological, behavioral and physiological characteristics during ontogeny (Mushinsky 1987).Alternatively a small percentage of rattlesnakes feed almost exclusively on endothermic preys, like C. durissus (Salomão et al. 1995;Duarte 2003), C. horridus and C. molossus (Clark 2002).Klauber (1956) gathered these three species and another, C. basiliscus, in the "durissus group", to demonstrate this specialization.
Mammal specialization may be related to several life history strategies (Martins et al. 2002).In some species of pitvipers, it could be associated with the increased venom toxicity in juveniles; this may be a consequence of the need to immobilize larger prey such as a mammal (Andrade & Abe 1999).Furthermore, the adoption of a juvenile diet based on mammals is more profitable energetically than an ecthothermic diet (Martins et al. 2002).In Crotalus durissus populations, the low frequency of ectothermic prey could explain such eventual facts.
Given this, behavioral and physiological changes necessary to switch from finding and consuming relatively sedentary ectotherms to finding and consuming fast, active endotherms might be costly (Clark 2002).Moreover, the microhabitat to which similar species are adapted to may not be used by local populations of reptiles that could serve as appropriate prey (Reinert 1984).
Several authors, point out the endothermic preys as a determinant element in food composition of C. durissus.For example, Beebe (1946) indicated that a specimen of this rattlesnake from Guyana contained a spiny rat.In populations from Uruguay, Achavál et al. (1978) reported that this rattlesnake commonly feeds on Cavia pamparum.Sant'Anna & Abe (2007), studying populations of southeastern Brazil, we observed that some species of rodents of the Caviidae and Muridae families followed by marsupials of the group Didelphidae, were the items most frequently consumed in this region.
In the current study, the diet composition of C. durissus was similar, characterized by a greater proportion of rodents.This mammals' group is terrestrial, nocturnal and dwell in open areas but they can also be found in forests (Emmons & Feer 1990;Nowak 1991).Similarly, in Cerrado endothermic prey types are rich and abundant, about 194 species of mammals are recognized, in which 51 are rodents and 17 marsupials (Marinho-Filho et al. 2002).This number has increased with the description of new species and the expansion of occurrence area of others (Bonvicino et al. 2003;Bonvicino et al. 2010).
In C. durissus, juveniles and adults feed predominantly on rodents (Sant'Anna & Abe 2007), a pattern attributed to the overall availability of this type of prey (Salomão et al. 1995).Field work confirmed an absence of ontogenetic variation in the diet which indicated that the juveniles of this rattlesnake could survive in dry locations with a supply    of rodents (Tozetti & Martins 2008).The consumption of rodents in all age classes and both sexes is favored because this prey is the most abundant throughout the year.Yet teid lizards (Ameiva) (Santos & Germano 1996) can be a sporadic food item in rattlesnakes.The teid Ameiva ameiva, is relatively abundant in Cerrado sites (Araujo & Almeida-Santos 2012) and even near human settlements (Colli et al. 2002), usually occupying similar habitats to Crotalus durissus.This could be one of the reasons that this species is more frequently consumed rather than other ectothermic prey.
Additionally, some factors such as adaptations related to competition, niche utilization, foraging strategies, costs of time and energy and prey availability (Schoener 1969;Shine 1986;Shine et al. 2002), could reflect important characteristics in the understanding of feeding ecology of C. durissus from the central region of Brazil.

Figure 1 .
Figure 1.Geographical distribution of Crotalus durissus with stomach contents from Central Region of Brazil covering forest formations of Amazon and Atlantic forest, Caatinga and Cerrado.