ANIMAL BEHAVIOUR, 2005, 70, 715–721 doi:10.1016/j.anbehav.2005.01.002 Does foraging mode influence sensory modalities for prey detection in male and female filesnakes, Acrochordus arafurae? S H AWN E. VIN CEN T*†, RI CH AR D SH IN E† & G REGORY P. BR OWN † *Department of Ecology & Evolutionary Biology, Tulane University ySchool of Biological Sciences, University of Sydney (Received 10 August 2004; initial acceptance 28 October 2004; final acceptance 4 January 2005; published online 6 July 2005; MS. number: A9965) Theoretical models predict that modalities of prey detection depend upon foraging modes: ambush foragers will rely on visual cues to launch a strike whereas active searchers will use chemical cues to locate prey. Testing this prediction is hampered by phylogenetic conservatism; ideally, we need to compare closely related animals that differ in foraging mode. Aquatic filesnakes from tropical Australia offer a unique opportunity of this kind, because female filesnakes ambush large fish in deep water whereas male filesnakes search actively for smaller fish in shallow water. We exposed freshly captured filesnakes to artificial prey items providing visual and/or chemical cues and measured tongue-flick rates and feeding responses of the snakes. Males responded most intensely to fish scent, regardless of movement, whereas females responded strongly to movement. Thus, our data provide the first intraspecific (sex-based) evidence for a functional relationship between foraging mode and the types of cues used for prey detection. Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Most species of animals can use information gained through a variety of sensory modalities such as vision, scent, sound, vibration and thermal cues (Krebs & Davies 1993). However, species differ enormously in their relative sensitivity to different kinds of stimuli. For example, most snakes have limited auditory acuity but some possess remarkably sensitive thermal receptors that allow them to detect warm-blooded prey, whereas many lizards have keen hearing but (as far as we know) cannot locate potential prey by using minor thermal differentials (de Cock Buning 1983; Greene 1997; Pianka et al. 2003). The degree to which a given species relies upon particular sensory modalities in its day-to-day life to locate prey, evade predators, find suitable mates, and so forth, depends upon a range of factors including its morphology, habitat and mating system (Foster & Endler 1999; de Queiroz 2003). However, one of the most clear-cut influences upon utilization of alternative sensory modalities involves foraging mode. Carnivores locate and recognize potential prey items by multiple cues, but the relative importance of specific Correspondence: S. E. Vincent, Department of Ecology & Evolutionary Biology, Tulane University, New Orleans, LA 70118, U.S.A. (email: svincent@tulane.edu). R. Shine and G. P. Brown are at the School of Biological Sciences, University of Sydney, Sydney, NSW 2006, Australia. 0003–3472/05/$30.00/0 sensory modalities may be affected by a primary dichotomy in foraging tactics. This issue has attracted considerable research in reptiles. Although there is broad recognition that any simple dichotomy is arbitrary, many authors have suggested that living squamate reptiles (lizards and snakes) can be broadly divided into two major foraging modes: ambush predators (also called ‘sit-and-wait foragers’) that lie in wait for their prey, versus active searchers. Extensive work suggests that reptilian ambush foragers tend to rely upon visual and thermal cues as stimuli to launch a strike (e.g. Greenwald 1974; Kardong & Smith 2002; Shine & Sun 2003) whereas chemoreception provides the most critical information about prey items for active searchers (Cooper & Vitt 1989; Kardong & Smith 1991; Cooper et al. 1994, 2000, 2002a, b; Cooper 1995; Shivik & Clark 1997; Shivik 1998). This pattern has generally been interpreted in terms of the kinds of cues available: an active searcher has access to the long-lasting chemical evidence of movements by a potential prey item and can use that information to track the prey, whereas an ambush predator must remain still and hence is forced to rely upon cues that provide immediate information about the prey’s proximity (see Shafir & Roughgarden 1998 for an overview). This hypothesis of a functional link between foraging modes and sensory modalities used for prey detection predicts that ambush predators will respond to visual cues, and active searchers to chemical cues. Ultimately, the 715 Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 716 ANIMAL BEHAVIOUR, 70, 3 critical test of this hypothesis requires comparisons between taxa that differ in foraging mode. Unfortunately, foraging modes show strong phylogenetic conservatism within most reptile lineages, as they do in the majority of animal lineages (Perry & Pianka 1997; Perry 1999), so that, perforce, the comparisons must involve taxa that differ in many respects other than foraging mode. Such confounding variables weaken any attempt to discern functional relationships between the variables of interest (Harvey & Pagel 1991; Garland et al. 1993). One solution to this problem is to identify phylogenetic shifts in foraging mode within major lineages, and look at the kinds of cues used for prey location by sister taxa that differ in foraging mode (Cooper 1995). However, such cases may be difficult to find; for example, a recent review (Beaupre & Montgomery, in press) laments that ‘due to the highly conserved nature of foraging mode within taxonomic groups, and the lack of specific knowledge regarding foraging mode and phylogeny, it is difficult to find circumstances that allow comparisons of behaviour, physiology and morphology between alternative foraging modes in sympatric, closely related snakes’. However, a species of tropical snake offers the strongest possible comparison: between the sexes within a single population. Arafura filesnakes not only display a greater degree of sex-based dietary divergence than has been documented in any other snake species, but field surveys suggest that the sexes also differ in foraging mode. Female filesnakes grow much larger than males, and ambush large fish in deep water. In contrast, the males actively move about in the shallows in search of small sleeping fish (Shine & Lambeck 1985; Shine 1986; Houston & Shine 1994). Radiotelemetric monitoring, direct observation and habitat-specific trapping have shown that male filesnakes travel long distances (albeit slowly) along the flooded margins of water bodies in search of small prey (Shine & Lambeck 1985). In contrast, traps set in deep water catch primarily large adult female filesnakes, which take much larger prey (Shine 1986). The location of foraging sites and the type of prey suggest that female filesnakes capture many of their prey from ambush positions (Shine 1986; see also Lillywhite 1991). However, there are no direct field observations of filesnake behaviour in deep water, because of the presence of saltwater crocodiles; thus, ambush predation by females remains an inference rather than a firm conclusion. We predict that if foraging modes are functionally linked to the use of alternative sensory modalities for prey detection, female filesnakes will rely primarily upon visual or vibrational cues to locate fish whereas males will rely primarily upon chemical cues. We set out to test this prediction. MATERIALS AND METHODS Study Species, Study Area and Methods of Collection We captured 17 filesnakes (5 males, 12 females, total size range 35.5–113.5 cm snout–vent length, SVL) by hand from a single site on the Adelaide river floodplain in the Northern Territory of Australia during the late wet season (February–March: Brown & Shine 2002), and subsequently housed the snakes outside in a shaded area (near where the snakes were captured) in separate 151-litre aquaria. Snakes were not fed for 2 weeks prior to behavioural trials; in the wild, such intervals between successive meals are common (see Houston & Shine 1994). The sex of each animal was determined by hemipenial probing (Fitch 1987). Trials Snakes were tested within their own aquarium (not transferred to a different testing aquarium) to minimize the time needed for snakes to acclimatize to their surroundings. As Arafurae filesnakes are highly nocturnal (Shine & Lambeck 1985), all trials were conducted between dusk and midnight. Each trial included a visual stimulus consisting of a 50-mm-long fishing lure in the shape of a sleepy cod, Oxyeleotris lineolata, a natural prey item for both sexes of Arafura filesnakes (see above). At the commencement of a trial the lure was placed directly behind the snake, out of its field of vision; and the lure was kept in one place throughout the duration of the trial. Each snake was tested twice, in random order, against each of the following six treatments: (1) fishing lure with no movement, (2) fishing lure C movement but no scent, (3) fishing lure C fish scent (derived from a frozen sleepy cod) but no movement, (4) fishing lure C fish scent C movement, (5) fishing lure C ham scent but no movement (derived from deli-sliced ham), and (6) fishing lure C ham scent with movement. Movement was produced by bobbing the lure up and down via a fine wire tied around the midbody of the lure. Scent was introduced by rubbing both sides of the lure alongside a frozen fish, until the researcher could easily detect the scent of fish on the lure. Trials lasted 5 min, timed using a stopwatch. Snakes received two treatments per day (one treatment with no movement, and one with movement of the same kind, e.g. fish scent alone in one trial, and a second with fish scent C movement). Aquaria were cleaned between different trial types so that lingering scents would not confound subsequent trials. Once all snakes had received all treatments, the experiment was replicated. For each trial, we recorded both the number of tongue flicks and the snake’s response to the stimulus. We categorized responses into the following types: (1) no overt reaction, (2) increase in rate of tongue flicking, but no orientation to the stimulus, (3) increased tongue flicking and orientation to the stimulus, or (4) attack (i.e. attempt to swallow or strike at the lure). Orientation was scored as whether or not the snake moved its head directly towards the lure during the trial. Statistical Analysis Data on the number of tongue flicks were log10 transformed to meet the assumption of homoscedascity prior to statistical analysis (Sokal & Rohlf 1981). We conducted three kinds of analyses. First, to examine whether tongue flicks offer a valid measure of prey detection, we compared VINCENT ET AL.: PREY DETECTION IN FILESNAKES variable) and the number of tongue flicks. In the majority of these cases (13/17), the result was statistically significant (P ! 0.05), and the other cases, while not reaching that level of significance, suggested the same trend. Although Bonferroni correction for multiple testing would modify the exact number of cases falling below specific significance levels, the consistency of this pattern clearly suggests that tongue-flick rates are functionally associated with prey recognition. The repeated measures ANOVA on mean rates of tongue flicking showed that male filesnakes tongue-flicked more often than did females (F1,15 Z 4.74, P ! 0.05) and that tongue-flick rates differed among the experimental trials (F5,75 Z 20.24, P ! 0.0001). More importantly, there was a significant interaction between sex and treatment (F5,75 Z 3.33, P ! 0.01) as a result of sex divergence in responses to scent versus movement (Fig. 2). The most critical trials were those with fish scent present: females responded most strongly if the lure was in motion, whereas males responded just as strongly to a motionless 200 (a) Female Male Mean tongue flicks tongue-flick rates among and within individuals as a function of their overt behavioural responses to the experimental stimuli. If tongue-flick rates are functionally associated with prey detection, we expect that snakes that show overt feeding behaviour will do so after displaying higher tongue-flick rates than individuals that do not launch a feeding strike. If tongue flicks are just a reflection of general level of arousal, we would not expect to see such a relationship. Second, we compared tongue-flick rates in response to different stimuli in male and female filesnakes. Because each individual snake was used in multiple trials, we cannot treat these data as statistically independent. Thus, we used repeated measures ANOVA with stimulus type as the repeated measure on (1) the mean number of tongue flicks per individual per treatment, averaged across the two replicate trials of that treatment for that snake; and (2) the maximum number of tongue flicks performed by each individual snake in response to each treatment type. To examine where differences reside among treatments, we performed Fisher’s protected least significant difference (PLSD) post hoc tests. Third, we used logistic ordinal regression to examine the role of prey movement and scent in eliciting feeding responses in male and female filesnakes. The ordinal dependent variable was the maximal response (in order: none, increased tongue flicking, orientation to prey, attack) for each snake to each stimulus, and the independent variables were whether or not the prey was moved and whether or not it provided scent cues. The larger sample size for females allowed us to repeat this analysis with body size (SVL) as an additional independent variable. 150 100 50 RESULTS Number of tongue flicks 200 N = 16 150 0 250 (b) Maximum tongue flicks Tongue-flick rates were relatively low in undisturbed snakes (i.e. prior to trials), and in animals that showed no overt reaction to the stimulus (Fig. 1). However, attacks on the lure consistently were preceded by high rates of tongue flicking (Fig. 1; ANOVA with snake behaviour as a factor: F3,16 Z 140.11, P ! 0.0001). All of the 17 individual snakes tested showed positive Spearman rank correlation coefficients between response level (an ordinal 200 150 100 50 100 N = 34 0 50 N = 117 N = 23 0 No reaction Tongue–flick Orient Attack Figure 1. Number of tongue flicks by filesnakes during 5-min observation periods, compared to the snake’s other behavioural responses to experimental stimuli. Data combined for all trials. Still Move Still Move Still Move Fish scent Ham scent No scent Figure 2. Mean G SE number of tongue flicks performed by male (N Z 5) and female (N Z 12) filesnakes in response to experimental stimuli (plastic fishing lures) that provided cues associated with movement (still versus move) and scent (none versus ham versus fish). (a) Mean values averaged across two replicate trials per treatment for each snake. (b) Maximum values recorded for each animal. 717 718 ANIMAL BEHAVIOUR, 70, 3 lure as to a moving one (Fig. 2). Fish scent increased the intensity of the males’ response more than that of the females’ response (Fig. 2). Almost identical conclusions were generated by analysis of data on maximum rather than mean rates of tongue flicking (Fig. 2; sex effect: F1,15 Z 6.45, P ! 0.03; treatment effect: F5,75 Z 23.88, P ! 0.0001; interaction between sex and treatment: F5,75 Z 4.63, P ! 0.001). Post hoc (Fisher’s PLSD) tests clarified the location of significant differences among treatments. Moving lures stimulated higher tongue-flick rates than did identical stationary lures in most comparisons (within each of the three categories of no scent, ham scent and fish scent: P ! 0.05 in post hoc comparisons between still and moving lures, for both mean and maximum tongue-flick rates). The sole exception to this pattern involved male snakes responding to trials that included fish scent, in which case movement induced a slight decrease rather than increase in tongue-flick rates (Fig. 2). Scent also influenced snake responses. The ham scent was not significantly different from the control treatment in this respect (control versus stationary stimulus: maximum tongue-flick rate: P Z 0.92; average tongue-flick rate: P Z 0.87; control versus moving stimulus: maximum tongue-flick rate: P Z 0.87; average tongue-flick rate: P Z 0.59) but fish scent induced much higher tongueflick rates (Fig. 2). Trials that included fish scent generated higher response rates than trials that did not involve fish scent (all P ! 0.05 in post hoc tests), albeit to a greater degree in males than females. Last, the ordinal logistic regression showed that for male filesnakes, prey scent was the most important cue eliciting a feeding response (likelihood ratio test: c22 Z 11.01, P ! 0.005), with no significant effect of prey movement (c21 Z 0.29, P Z 0.59) nor any significant interaction between these prey attributes (c22 Z 0.35, P Z 0.83). In contrast, feeding responses of female filesnakes were affected by prey movement (c21 Z 6.42, P ! 0.02) as well as scent (c22 Z 16.23, P ! 0.001), again with no significant interaction between these two types of cues (c22 Z 1.88, P Z 0.39). Because of the larger sample size for females, we then repeated the analysis after including snout–vent length as a factor. The expanded analysis revealed a significant effect of SVL on response (c21 Z 7.59, P ! 0.01) but more importantly, an interaction between movement cues and SVL (c21 Z 7.13, P ! 0.01). Overall, larger females were less likely than smaller females to respond to stimuli, but especially to movement cues. Thus, the greatest difference in importance of movement cues was between males and small females, the two groups most similar in body size. DISCUSSION The sex divergence in dietary composition, foraging habitats and foraging modes within Arafurae filesnakes is accompanied by sex divergence in the cues that elicit feeding responses. Consistent with theory-based foraging models and with the results of interspecific comparisons on other kinds of reptiles, our intraspecific comparison revealed a significant link between foraging modes and the relative importance of alternative sensory modalities. Male Arafura filesnakes appear to largely rely on fishspecific chemical cues during predation, whereas conspecific females show a greater reliance upon visual and/or vibrational cues (fish movement). The sex difference is one of degree rather than a strict dichotomy, because both males and females responded more strongly to stimuli that provided either movement or scent cues than to stimuli lacking those attributes. Nevertheless, the relative importance of those two types of cues differed between the sexes (Fig. 2). In keeping with size-related shifts in food habits within each sex, we also detected a significant size-related shift in the importance of prey movement cues for female filesnakes. Aquatic and semiaquatic snakes have been popular organisms for studies on the sensory modes involved in prey location. Most of this work has focused on a single major lineage, the natricine colubrids, and has taken place primarily in North America (e.g., Burghardt 1966, 1968, 1970; Drummond 1979, 1983, 1985; Arnold 1981; Halloy & Burghardt 1990; Rossman et al. 1996; Burghardt & Schwartz 1999; de Queiroz 2003) and Europe (Patterson & Davies 1982; Hailey & Davies 1986). Homalopsine colubrids from Asia (Jayne et al. 1988) and Australia (Shine et al. 2004) also have attracted study. Despite their diversity, most other lineages of aquatic snakes have been virtually neglected in this respect (but see Shine et al. 2003 for sea snakes). To our knowledge, ours is the first study of prey detection modalities in any acrochordid. The invasion of aquatic habitats by snakes from several major phylogenetic lineages (see Heatwole 1999; Cundall & Greene 2000; Alfaro & Arnold 2001) offers substantial opportunities to examine independent evolutionary solutions to the challenges involved in locating and capturing prey in this novel environment. The aquatic medium is a particularly interesting environment for prey capture by snakes due to the high viscosity and density of water (relative to air) and given that snakes cannot generate compensatory suction, unlike most aquatically feeding tetrapods (Lauder 1985; Cundall & Greene 2000). Aquatic snakes have evolved an impressive array of aquatic prey capture and detection behaviours (see Drummond 1983; Smith et al. 2002), which were once thought to vary only interspecifically (Drummond 1985). By contrast, we show here that aquatic prey detection behaviours can vary even within a single species. The highly labile nature of these foraging behaviours suggests that aquatically feeding snakes represent an ideal system to study adaptation at various phylogenetic levels. Moreover, as molecular phylogenies have recently become available for many groups containing aquatically feeding species (i.e. natricines and homolapsines, see Alfaro & Arnold 2001; Voris et al. 2002), robust phylogenetic methods can now be applied to shed significant light on the evolution of aquatic feeding within snakes. Sympatry is frequent in aquatic snakes, so that a single field study potentially could examine representatives of multiple, phylogenetically independent invasions of aquatic habitats. For example, mangrove areas in Asia and Australasia often contain sympatric hydrophiids, laticaudids, homalopsine colubrids and acrochordids VINCENT ET AL.: PREY DETECTION IN FILESNAKES (Voris et al. 1978; Voris & Jane 1979; Voris & Glodek 1980; Voris & Moffett 1981; Voris & Voris 1983; Heatwole 1999). Even when dietary composition is similar among such taxa, foraging behaviours may differ. The present study offers an example of such divergence. Our data suggest that male acrochordids use chemical cues to locate sleeping fish in the shallows, whereas a homalopsine colubrid species that lives in the same habitats and feeds on many of the same species of fish, locates fish prey primarily using visual and tactile cues (Shine et al. 2004). More generally, intraspecific divergence in foraging biology offers considerable opportunities to examine causal links without the confounding issues inevitably introduced by interspecific (or even, interpopulation) comparisons (Harvey & Pagel 1991; Perry 1999; see Herrel et al. 2002 for an example of interpopulation divergence). Intraspecific niche divergence is widespread among snakes: not only do males and females frequently differ in diet and trophic morphology (i.e. head dimensions), but the same is true also for comparisons between juveniles and adults (Shine 1991; Shivik & Clark 1999; Shine & Wall, in press a, b; Vincent et al. 2004). Thus, individuals within a single population may vary greatly in terms of the kinds of prey they consume, the times and places where they obtain those prey, and the foraging behaviours by which they procure their food (Shine & Wall, in press a, b). For example, the aquatic strike behaviour (lateral versus frontal strikes) used by many natricine snakes is often context dependent (e.g. it is influenced by the depth of fish within the water column) and the propensity to perform particular feeding behaviours varies among individuals within a population (Rossman et al. 1996; de Queiroz 2003; Bilcke et al., in press). Ontogenetic, seasonal and facultative shifts between ambush predation and active foraging have also been reported in many reptile species (e.g. Taylor 1986; Rodda 1992; Li 1995; Shivik et al. 2000). Similar opportunities for intraspecific comparisons can be found in other study systems also, because it will often be true that an individual’s body size, sex or location influences the types of food that it obtains, and the ways in which it locates and subdues those prey items. For example, differences in feeding structures (jaws, teeth, etc.) between conspecific males and females have been reported in a diverse array of animal taxa (Shine 1989). Some of these cases reflect sex-based divergences in reproductive behaviour (e.g. male–male combat), but many cases appear to be adaptations to sex-based dietary partitioning (Shine 1989). This situation provides abundant opportunities for tightly focused comparisons between males and females within a single population to explore the ways in which ecological traits (such as foraging mode) influence the relative importance of alternative sensory modalities during foraging. Acknowledgments Experimental procedures were approved by the University of Sydney Animal Ethics Committee (Approval Number: L04/5-2004/1/3888). We thank Anthony Herrel for shar- ing his unpublished data on European natricines, and Simon Lailvaux and Duncan Irschick for comments on the manuscript. 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