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Relationship of Venom Ontogeny and Diet in Bothrops

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Relationship of Venom Ontogeny and Diet in Bothrops Herpetologica. 55(2), 1999, 200-204 @ 1999 hy The Herpetologists' League, Inc. RELATIONSHIP OF VENOM ONTOGENY AND DIET IN BOTHROPS DENIS V ANDRADE AND AUGUSTO S. ABE Departamento de Zoologia, Universidade Estadual Paulista, c. p. 199, 13506-900, Rio Claro, São Paulo, Brazil ABSTRACT: We studied ontogenetic changes in venom toxicity of the pitvipers Bothrops jararaca and B. altematus in order to evaluate the relationship between venom action and diet. Toxicity tests (LD",,) were performed for the venoms of adult and juvenile snakes on mice and bullfrog froglets, which represented endothermic and ectothermic prey respectively. The venom of juveniles of B. jararaca, but not of B. altematus, had a higher toxicity on anurans than that of adults. This finding is consistent with the feeding habits of these two species, because juveniles of B. jararaca feed mainly on small anurans and lizards, shifting to endothermic prey at maturity, whereas B. altematus preys mainly on endotherms throughout its life. Venom toxicity in endotherms was higher for adults of B. jararaca compared to juveniles, a feature not observed for B. altematus. It is proposed that prey death!immobilization is the main function of the venom of juvenile snakes. As the snake grows, the digestive role of venom may become increasingly important, because adults prey upon large and bulky prey. The importance of adult venoms in prey digestion is reflected in their higher proteolytic activity. Key words: Bothrops; Electrophoresis; Venom ontogeny; Venom specificity; Viperidae SNAKESare strictly camivorous and al- that ontogenetic variation could be related ways ingest their prey whole, and for many to differences between the feeding habits species feeding episodes occur sporadical- of juvenile and adult snakes (Gans and EI- ly on relatively large animals (Greene, liot, 1968; Sazima, 1991). In this study, we 1983, 1997). Juvenile and adult snakes of- tested the association between venom on- ten show differences in body size and oth- togeny and diet for two species df the pit- er behavioral, morphological, and physio- viper genus Bothrops. This genus is com- logical characteristics that may lead to an posed of species that change their diet ontogenetic shift in diet (Mushinsky, during growth (Martins and Gordo, 1993; 1987). In a number of snakes, such dietary Sazima, 1991, 1992; Sexton, 1956-1957) shifts are characterized by juveniles prey- and that feed mainly on endotherms ing primarily upon ectotherms while adults throughout their life (Andrade, 1995; M. feed mainly on endotherms (Mushinsky, Martins, personal communication), mak- 1987; Saint-Girons, 1980; Sexton, 1956- ing it possible to examine the relationship 1957). between the ontogeny of venom and diet. Diet shifts are widespread among viper- To evaluate the possible correlations be- ids, a group of snakes in which prey cap- tween venom toxicity and prey type, we ture is largely dependent on a parenteral tested venoms of juveniles and adults of venom injection (Greene, 1992). Viperid Bothrops for their effectiveness in frogs venoms are among the most complex and and mice, which represent ectothermic variable substances secreted by vertebrates and endothermic prey, respectively. (Gans and Elliot, 1968), varying specifical- Among Bothrops exhibiting ontogenetic ly (Bemadsky et al., 1986; Tan and Pon- shifts in diet, we studied the venom of B. nudurai, 1990a,b; Wüster and Thorpe, jararaca, a medium-sized (approximately 1991), geographically (Daltry et al., 1996; 100 cm snout-vent length: SVL), relatively Glenn et al., 1983; Jayanthi and Gowda, slender pitviper widespread in southeast- 1988), seasonally (Gubensek et al., 1974; em Brazil (see Sazima, 1992, for natural Ishii et al., 1970), and ontogenetically history). Among Bothrops that feed on en- (Dempfle et al., 1990; Lomonte et al., dotherms throughout life, we investigated 1983; Meier, 1986). It has been proposed the venom of B. altematus, a large, heavy- 200 June 1999] HERPETOLOG1CA 201 bodied snake growing up to 160 em SVL TABLE 1.-Toxicity (LD.;o) of the venoms of adults (Andrade, 1995; Campbell and Lamar, and juveniles of Bothrops jararaca and B. altematus 1989). in mice and frogs (mglkg); 95% confidence limits in parentheses. MATER1ALS AND METHODS Mice Frogs Snakes and Venom Samples Bothrops jararaca Individuals of B. jararaca were eolleeted Juvenile venom 5.88 53.64 at several loealities in São Paulo State, (4.6-7.31) (44.04-65.99) Adult venom 1.74 91.44 southeastem BraziI. Speeimens of B. alter- (1.26-2.2) (73.lI-lI4.79) natus were eolleeted in Botueatu, São Pau- Bothrops altematus lo. Venoms from juveniles of B. jararaca Juvenile venom 4.54 79. II and B. altematus were obtained mainly (3.56-5.86) (65.03-99.2) from the offspring of females kept in eap- Adult venom 4.69 77.53 tivity. (3.49-6.44) (63.73-97.22) Venom samples of B.jararaca were eol- leeted from juveniles «45 em SVL), sub- adults (45-80 em SVL), and adults (>80 to prevent temperature effeets on meta- em SVL). These age classes refleet ap- bolie rate (Witford, 1973) which eould af- proximately the size at which diet ehanges feet the aetion of the venom. in this speeies, with juveniles feeding mainly on eetotherms, adults on endo- RESULTS therms, and sub-adults making the transi- Venoms from adults ofboth B.jararaca tion between both diets (Andrade et al., and B. altematus as well as juveniles of B. 1996). For eomparative purposes, the altematus did not differ markedly in their same size-based separation was applied to LDso values in frogs (Table 1). Conversely, B. altematus, regardless that its diet does the toxicity of juvenile venom from B. ja- not ehange. raraca in frogs was nearly twiee that ob- Venoms were extraeted manually, served for the venom of adults. For mice, pooled, and immediately vaeuum dried the venom of the adults of B. jararaca was and stored at -20 C. Storage never exeeed about 3.4 times more lethal than that of 10 mo after eolleetion. For alI toxicity juveniles, whereas for B. altematus, the tests, venom solutions were prepared im- toxieity of the venoms was similar in ju- mediately before use. veniles and adults. Toxicity Tests D1SCUSSION We determined lethal toxicity of the Toxieity data indieate that the venom of venoms in outbred Swiss-Webster miee juveniles of B. jararaca is especially effi- (18-22 g) and in juvenile bullfrogs (Rana eient on anurans. As the snake grows and catesbeiana, 5-10 g). We used five dose its diet ehanges, the venom of this species levels in eaeh toxieity assay. Dried venom loses about 70% of its toxieity upon the was diluted in 0.9% saline and injeeted in- preferred prey of the juvenile phase. Sim- traperitoneally (i.p.) in six animals at eaeh ilarly, in B. moojeni, which also ehanges its dose leveI. The volume injeeted was 0.5 ml diet from eetotherms to endotherms dur- for miee, but in frogs it was adjusted to ing ontogeny, the toxicity of the juvenile individual masses (0.025 ml of venom so- venom is about 86% higher for eetotherms lution for 1 g of frog) due to their larger than that of adults (Andrade et al., 1996). range of masses. Toxieity was expressed as Thus, in B. jararaca (this study), B. moo- lethal dose 50% (LDso) estimated using jeni (Andrade et al., 1996), and possibly the probit analysis following Finney other species of Bothrops that possess an (1971). We eonsidered mortality reeorded ontogenetie shift in diet, the toxieity of the up to 48 h treatment for miee and 72 h venom of juveniles eorrelates with their for frogs. AlI experiments with frogs were feeding habits. In eontrast, in B. altema- performed in a elimatie ehamber at 25 C tus, which feeds on endotherms at any 202 HERPETOLOGICA [VoZ. 55, No. 2 size, the venom of juveniles lacks an in- prey are taken (Greene, 1992; Sazima, creased toxicity on ectothermic organisms. 1992), and digestion becomes more diffi- Further investigation may reveal that this cult due to the greatly reduced surface to pattem extends to other heavy-bodied spe- volume ratio of the prey (Pough, 1983; cies of Bothrops, like B. cotiara and B.fon- Pough and Groves, 1983). At this point, secai, possessing ontogenetically flxed di- the selective pressures acting on venom ets. composition may shift, and its function in For miee, the venom toxicity of adults prey digestion may become increasingly of B. jararaca is 2.3 times higher than that important. Accordingly, increased prey di- of juveniles, reflecting a diet change to en- gestive resistance leads to a concurrent in- dothermic prey. For B. altematus, which crease in venom proteolytic activity (An- feeds on endotherms both as juvenile and drade et al., 1996; Mackessy, 1988), a fea- adult, the venom of juveniles is expected ture also observed for B. jararaca and B. to have a higher toxicity on endotherms to altematus (Furtado et al., 1991). As the compensate for its smaller volume. How- venom is injected into the prey's body, ever, we found no difference in the toxicity higher proteolytic activity associated with of juvenile venom from B. altematus and injection of a greater volume (Hayes et al., that of adults. Therefore, a clear relation- 1995) could accelerate the rupture of tis- ship between venom toxicity in endo- sues, increasing the prey surface area ex- therms and feeding habits is not apparent posed to stomach acids and enzymes in the species of Bothrops presently stud- (Thomas and Pough, 1979). Enhancement ied. In general, the amount of venom of prey digestion may reduce time and en- spent by a snake to capture an endother- ergy allocation, shortening the period in mie prey item is small (Hayes, 1991; Hayes which snakes have their capacity for loco- et al., 1995) compared to the quantity pro- motion and defense decreased (Ford and duced by an adult or even a juvenile snake Shuttlesworth, 1986), and lowering the (Furtado et al., 1991).
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