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Defensive Behaviour in Pit Vipers of the Genus <I>Bothrops</I

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Defensive Behaviour in Pit Vipers of the Genus <I>Bothrops</I HERPETOLOGICAL JOURNAL, Vol. 16, pp. 297-303 (2006) DEFENSIVE BEHAVIOUR IN PIT VIPERS OF THE GENUS BOTHROPS (SERPENTES, VIPERIDAE) MÁRCIO S. ARAÚJO1 AND MARCIO MARTINS2 1Programa de Pós-Graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brazil 2Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil The genus Bothrops encompasses at least six evolutionary lineages that show a great diversification in macro and microhabitat use. We studied the defensive behaviour of one species of each of five lineages within the genus Bothrops: B. alternatus, B. jararaca, B. jararacussu, B. moojeni and B. pauloensis. Specifically, we investigated if this diversification in habitat use was accompanied by a similar divergence in the characters related to defensive behaviour in the genus. Eight behavioural categories were recorded, five of which may be classified as “threatening” (strike, tail vibration, head and neck elevation, dorsoventral body compression and body thrashing); two as “escape” (locomotor escape and cocking); and one as “cryptic” (head hiding). We observed significant differences in four behavioural categories. We also detected a significant difference in the way species elevated their head and neck. Tail vibration and strikes were the most common behaviours presented, and snakes that displayed their tails struck more frequently than those that did not display. A reconstruction of characters related to defensive behaviour on a phylogeny of Bothrops indicated an increase in the use of dorsoventral body compression in the groups alternatus and neuwiedi, which may be associated with the invasion of open areas by these lineages. Key words: comparative method, Crotalinae, defensive tactics, evolution of behaviour INTRODUCTION The genus Bothrops (including Bothriopsis; e.g., Snakes are exposed to different kinds of predators in Wüster et al., 2002) includes about 45 described spe- the various habitats they occupy (Greene, 1988), and, as cies (Campbell & Lamar, 2004). The phylogenetic a result, may differ in defensive behaviour. For example, relationships within Bothrops have been explored in snakes in open habitats may suffer a more intense preda- the last few years (e.g. Salomão et al., 1997; Vidal et tion pressure from highly mobile predators than in al. 1997; Wüster et al., 2002). The genus encompasses forested habitats (Greene, 1988). Microhabitat use in at least six lineages, the groups atrox, jararacussu, snakes (e.g. terrestrial, arboreal) may also be associated jararaca, alternatus, neuwiedi and taeniatus (Wüster with defensive behaviours (Greene, 1979). For instance, et al., 2002). an association between gaping behaviour and arboreality Here we describe and compare the defensive behav- has been demonstrated in snakes (Greene, 1997). In the iour of one species of each of five lineages within the case of the genus Bothrops, the ways by which the habitat genus Bothrops, namely B. alternatus (alternatus is used by snakes are diverse (Martins et al., 2001). group), a terrestrial species which inhabits open areas; Within the genus, there are lineages of both open and B. jararaca (jararaca group), a semi-arboreal forest forested areas and with varying degrees of arboreality dweller; B. jararacussu (jararacussu group), a terres- (Martins et al., 2002). These differences in use of trial forest inhabitant; B. moojeni (atrox group), a microhabitat (terrestrial and arboreal) and macrohabitat semi-arboreal species found in open formations, but (open and forested areas) may be associated with differ- associated almost exclusively with riparian forests ences in defensive behaviour of the different lineages of within these areas; and finally B. pauloensis (neuwiedi Bothrops. In fact, with the exception of the studies on B. group), a terrestrial species exclusive to open areas jararaca by Sazima (1988, 1992), there are no detailed (Table 1). We also explore the evolution of characters studies of defensive behaviour in the genus Bothrops. related to defensive behaviour in the genus Bothrops Sazima (1992) suggested that comparative studies and speculate on possible associations between among some Bothrops species typical of forested areas changes in defensive behaviour and changes in habitat and species of open areas could reveal similarities and use. differences related to their ecology and their MATERIALS AND METHODS phylogenetic relationships. Test subjects were species of Bothrops from several localities of southeastern (B. alternatus, B. jararaca, Correspondence: M. S. Araújo, Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de B. jararacussu, B. pauloensis and B. moojeni) and cen- Campinas, CP 6109, 13084-971, Campinas, SP, Brazil. tral Brazil (B. moojeni) brought to the Instituto E-mail: [email protected] Butantan between April 1998 and February 1999. Ten 298 M. S. ARAÚJO AND M. MARTINS TABLE 1. Habitat use, sizes (mm), captivity duration (days), and number of individuals of the five species of Bothrops studied. T: terrestrial; SA: semi-arboreal; O: open areas; F: forests; SVL: snout–vent length; SD: standard deviation; CD: captivity duration; n = number of individuals. Species Habitat use Mean SVL SD Mean CD SD n B. alternatus T/O 708.6 160.35 4 4.8 10 B. jararaca SA/F 803.2 169.86 1 1.3 10 B. jararacussu T/F 611.1 187.13 8 9.6 10 B. moojeni SA/F 946.5 137.48 5 3.6 10 B. pauloensis T/O 608.0 126.23 5 2.8 10 individuals of each species were tested as they arrived at Defensive behaviour was elicited with using a stimu- the Instituto Butantan (Table 1). Upon arrival, individu- lus object, a plastic bottle (height 15 cm; diameter 10 als were housed in a large plastic container (c. 100 × 70 cm; volume 0.5 l) covered with a 0.5 cm-thick sheet of × 60 cm high) with bark mulch as a substrate. Snakes soft black rubber to which a 1.5 m plastic pipe was at- were not manipulated until they were removed from the tached at a 45° angle. The purpose of the rubber was to container, measured and individually put in small wood minimize injuries to the snakes’ fangs during strikes. containers, and taken to a temperature-controlled labo- The bottle was filled with warm water (60oC) shortly ratory (25±2oC) where the tests were conducted. The before the tests to raise the temperature of the external snakes were taken to the laboratory during daytime, ap- surface of the rubber to about 37oC (mean±SD = proximately eight hours before the initiation of the tests, 37.1±0.94oC; n=17; recorded immediately before trials and the tests were carried out on the same day, always at by a Miller & Weber Inc. quick-reading thermometer night, from 1758 hr to 0002 hr. The snakes were tested with an accuracy of 0.1oC). The stimulus object was de- 0–16 days after arrival at the Instituto Butantan, except veloped by us and was chosen, among several others, on for one individual of B. jararacussu that was kept for 33 the grounds that it immediately elicited typical defen- days at the Instituto Butantan before tests were per- sive behaviours upon its introduction into the arena. We formed. Each individual snake was tested only once. believe that the stimulus object simulated the head of a The tests were carried out in an arena set on the mammal approaching the snake horizontally and close ground of the laboratory (Fig. 1). The laboratory wall to the ground. formed one of the sides of the arena; the other three Before each test, the internal surfaces of the arena as sides were made of wood and glass. One of the sides well as the stimulus object were cleaned with ethanol. adjacent to the wall was opaque and the other two sides The snake was then put in the centre of the arena and a were transparent. During trials, we stayed behind the transparent acrylic box (30 cm on each side and 15 cm opaque side of the arena to minimize possible distur- high), with the open side facing down, was put over the bance. Two Panasonic NVRJ PR VHS cameras were snake using a hook. We used a transparent box to make used, one over the arena set on a tripod and facing the sure that the snake could see its surrounding environ- ground, and the other on the ground, lateral to the arena ment before the initiation of trials. The acrylic box was and facing the wall. The ground was covered with a also cleaned with ethanol before the tests. The arena black plastic sheet; both the plastic sheet and the wall lights were on prior to introducing snakes into the arena. had gridlines of 1 and 2 cm, respectively, for distance Snakes were left undisturbed for 10 minutes before the estimates. The light sources were two 60 W bulbs set on beginning of the tests. The 10 minute interval was se- the main axis of the arena, one at each side. Although lected arbitrarily, but we believe it was enough for the rather artificial, the light sources were necessary for the snakes to settle down before the initiation of trials. recording of the trials on tape. Cameras were turned on by remote control and re- corded at 30 frames/s. Trials began when the acrylic cover was removed with a hook and the stimulus object was introduced into the arena and moved towards the snake, parallel to the ground and about 1 cm above it, always by the same person. The stimulus object touched the snake’s body and was withdrawn repeatedly, about once every two seconds, 30 times uninterruptedly for each snake. If the snake went out of the camera’s field (time out; cf. Martin & Bateson, 1993), the stimulus ob- ject was removed from the arena and the snake was brought to its centre with a hook; this will hereafter be termed an intervention.
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