How do water skinks avoid shelters already occupied by other lizards? Tracy Langkilde1) & Richard Shine2) (Biological Sciences A08, University of Sydney, NSW 2006 Australia) (Accepted: 1 February 2005)
Summary Animals rely on a wide range of sensory modalities to obtain information about their environment, and to determine the most appropriate behavioural response for a give situation. Scincid lizards use both chemosensory and visual cues in tasks such as mate location, shelter-site selection, and predator evasion. Published literature has focused primarily on the use of chemosensory information by these lizards, but our experiments reveal an alternative scenario. Water skinks (Eulamprus heatwolei) are sympatric with larger black rock skinks (Egernia saxatilis) in southeastern Australia, and use similar long-term retreat-sites. However, Eulamprus avoid shelter-sites occupied by Egernia because of the risk of attack and injury. We conducted laboratory trials to clarify the kinds of information used by Eulamprus to avoid already-occupied shelters. In the field, shelter-sites might provide three types of information about prior occupancy: either scent deposited by a previously present Egernia; evidence of the current presence of an Egernia, perhaps involving visual, chemical, and/or auditory information; or a direct behavioural interaction with a resident lizard (potentially involving an attack). In our trials, Eulamprus based their shelter-site avoidance only on direct interactions. Thus, Eulamprus reacted strongly to Egernia with which they were able to interact physically, but not to either Egernia scent deposits, or a (caged) Egernia with which they could not physically interact. The behaviour of the resident was critical, in that Eulamprus fled from the crevice in response to bites, movements, or open-mouth displays by the resident Egernia. We suggest that Eulamprus base their shelter-site choices on the presence of an actual resident animal rather than more indirect cues (such as scent), because only a direct encounter provides reliable information about the magnitude of threat associated with crevice occupancy. Keywords: interspecific aggression, habitat use, competition, avoidance, Egernia, Eulamprus.
1) 2)
Corresponding author’s e-mail address:
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© Koninklijke Brill NV, Leiden, 2005
Behaviour 142, 203-216 Also available online -
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Introduction Animals rely on a wide range of information about their surroundings to determine the most appropriate behavioural response to a particular situation. The types of information used may vary not only among major lineages, but also over brief timescales even for a single organism (Falkenberg et al., 2004; Shine et al., 2004). In general, we expect animals to rely upon information with the most useful content, and this in turn will depend upon issues related to communication effectiveness per se (e.g., signal fidelity, interference from background sources) as well as to the biological context (e.g., does the organism need to know another animal’s body size as well as its sex or species?: Dawkins & Guilford, 1994; Brumm et al., 2004). Alternative information sources often differ in both of these respects, allowing substantial opportunity for animals to rely upon different kinds of information in different situations. For example, frog species that breed in high-ambient-noise environments may rely upon visual rather than auditory signalling to choose mates (Haddad & Giaretta, 1999). Similarly, multiple sources of information can contribute in an additive way to facilitate a better informed decision about the level of risk than would be available from any single source (e.g., Bouwma & Hazlett, 2001; Smith & Belk, 2001). Squamate reptiles (lizards and snakes) obtain information about their environment from a variety of sensory modalities. For example, diurnal lizards employ visual signals such as head-bobbing and dewlap extension to maintain territories and court females (Jenssen, 1977; Wiens, 2000; Tokarz, 2002), whereas snakes rely on chemical cues to locate mates (Mason, 1992; Shine et al., 2003). One scenario especially amenable to experimental manipulation, and hence that has attracted considerable study, comprises the information that lizards and snakes use when selecting retreat sites. Several taxa have been shown to evaluate a range of attributes when selecting sheltersites. For example, snakes select sun-heated rocks with specific diel thermal cycles (Huey et al., 1989; Webb & Shine, 1998; Pringle et al., 2003) and both scincid and gekkonid lizards actively select among alternative retreats based not only on abiotic (thermal, hydric, structural) attributes, but also on the presence of conspecifics and potential predators (Schlesinger & Shine, 1994; Downes & Shine, 1998; Shah et al., 2003). Chemical signals from lizards and predatory snakes strongly influence microhabitat use in scincid, lacertid, and gekkonid lizards (Downes & Shine, 1998; Aragon et al., 2001; Van Damme & Quick, 2001; Head et al., 2002).
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Although published literature on retreat-site selection by lizards emphasizes the use of chemosensory cues, there may be circumstances in which organisms obtain more reliable and relevant information from visual inspection (Amo et al., 2004). This situation should occur especially if the critical question is not whether or not another animal has been present, but whether it is currently present and if so, how it is likely to behave towards the focal animal. Because scent can persist for long periods (especially in protected areas such as shelter-sites, Mason, 1992; Webb & Shine, 1992), deposited scent cues may be linked only weakly to the presence of the animal that produces that scent. In contrast, visual cues give immediate information not only about presence, but also about postures that may predict behaviour. Our study system consists of two species of viviparous scincid lizards that occur sympatrically, and at high densities, in the Kanangra-Boyd wilderness of southeastern Australia (Cogger, 2000). They utilize shelter-sites that are similar in most abiotic factors, but are warmer than surrounding unoccupied shelters (Langkilde et al., 2003). Shared occupancy of the same retreatsite was never observed; both field and laboratory observations suggest that this pattern is due to strong agonistic interactions between and within these species (Langkilde & Shine, 2004). Black rock skinks (Egernia saxatilis) attack smaller water skinks (Eulamprus heatwolei) that attempt to enter their crevices. In consequence, Eulamprus appear to avoid crevices occupied by Egernia, but will occupy these crevices in the absence of Egernia (Langkilde & Shine, 2004). We will refer to these species by their generic names hereafter for simplicity. A Eulamprus searching for a suitable retreat-site is likely to encounter three types of shelters in the field: (1) empty shelters, (2) empty shelters containing scent deposited by a previous resident, and (3) shelters containing a resident lizard. Plausibly, the Eulamprus might thus base its decision about whether or not to use that crevice upon (1) scent cues, even in the absence of a current resident (individual Egernia re-use the same crevices over long periods; O’Connor, 2003, so scent cues might indicate that the crevice, even if currently unoccupied, is home to an Egernia); (2) the presence of another lizard (via any of a range of sensory modalities, including scent, sound and vision); or (3) the behaviour of the current resident (i.e., the Eulamprus might remain in a crevice unless it is attacked, or threatened). We conducted replicated laboratory trials to test whether deposited scent elicited avoidance of shelters previously occupied by Egernia, or whether
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Eulamprus instead rely on more direct information gained from the resident itself (either its physical presence, or specific behaviours) when making this decision.
Methods Lizards used in our experiments were captured by hand from KanangraBoyd National Park 160 km west of Sydney, New South Wales (33◦ 58.207 S, 150◦ 03.346 E), and returned to the point of capture at the completion of trials. Shelter-site choice Each experimental enclosure (600 × 330 × 200 mm depth) contained two shelters (inverted plastic boxes with entry holes cut out of the far right-hand side of one wall to allow ingress of lizards: 130×130×20 mm depth), one of which was heated (using a sub floor heating strip) to 36◦ C whereas the other was maintained at 21◦ C. The remaining open area was maintained at 16◦ C. Previous work has shown that both Eulamprus and Egernia prefer the ‘hot’ shelter (Langkilde & Shine, 2004), so that a solitary lizard of either species when placed in the enclosure almost always selected the ‘hot’ shelter as its retreat. This set-up mimics the field situation; rocks used as shelter-sites by these species are significantly warmer than nearby unoccupied rocks (Langkilde et al., 2003). This also means that, in the field, warmer rocks are likely to be occupied, whereas cool rocks are likely to be unoccupied. We added male Egernia cues to the hot (‘preferred’) shelter and tested the preference of Eulamprus (N = 10 males, N = 10 females) for the ‘hot’ shelter site in four natural situations to provide the focal lizard with a choice between the cold shelter and either: (1) a hot shelter with no cues from Egernia; (2) a hot shelter scented by Egernia; (3) a hot shelter containing an Egernia that was behind a divider and thus could not interact physically with the focal lizard; or (4) a hot shelter containing a free ranging Egernia. In previous studies, a lizard’s sex did not affect its intensity of aggression (Langkilde & Shine, 2004). Therefore, we used only male Egernia as stimulus animals to reduce any potentially confounding effects. Shelters used in treatment (2) were kept in individual Egernia home cages for at least one week prior to use in the trials and were moved directly from
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these cages to the experimental enclosures for the trials, ensuring the scent was less than 5 minutes old at the initiation of the trials. Scent cues from separate individual Egernia were used for each trial. All shelters had plastic floors, and the ventral surfaces of the Egernia came into contact both with the floor of the shelters and with the external roof of the shelters, as they often used them as a basking platform. We are confident that detectible quantities of chemical cues were transferred to these shelters; large quantities of shed skin and scats accumulated on and inside these shelters over the 7 or more days, and the resulting scent was detectable even by relatively insensitive human noses. Shelters used in treatment (3) were divided in half diagonally with thin plastic mesh (mesh size 5 × 5 mm square), with an Egernia housed in the half of the shelter not containing the entry hole. This enclosed portion was large enough for the Egernia to move around, and the positioning of the divider allowed the Egernia to move to within 5 mm of the entry hole. This set-up allowed the free transfer of information about the presence of the other lizard (e.g., visual, chemical, auditory), but prevented physical interactions between the two animals. In treatment (4), Egernia were placed under an undivided hot shelter, and hence were free to physically interact with the Eulamprus. Each individual Eulamprus was tested in each of the four treatments, in a maximum of two trials per day. Enclosures were cleaned between trials, and new shelters were used in each trial. The order of presentation of these treatments was randomized for each focal lizard. Different individual Egernia were used in each trial. A trial commenced when the focal Eulamprus was placed into the centre of the enclosure. Beginning 15 minutes later, and then again 60 minutes after the trial commenced, we recorded the location of the Eulamprus in the enclosure (either under the hot shelter, under the cold shelter, or in the open) four times at five-minute intervals. Preliminary analyses revealed no significant difference in the shelter use of individuals between these two time periods, so we report only the data collected in the second period, 60 to 75 minutes after the trials commenced. From these observations, we calculated the average number of times (of the four observations) that the Eulamprus were observed under the ‘hot’ shelter in each trial. The resulting data on the number of times individuals were observed under the hot shelter in each of the treatments were analyzed with ANOVA followed by Tukey posthoc tests.
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Latency and stimulus to flight We conducted video trials to quantify the lizards’ latency to flee from shelters providing different information, and to explore behaviours of both participants in more detail. We used male Eulamprus (N = 10) as focal animals and male Egernia (N = 10) as stimuli in these trials. Eulamprus were presented with the same four experimental treatments as described above (control, scented, Egernia in divided shelters, Egernia in undivided shelters) but without the cold shelter. For the trials involving Egernia, these lizards were introduced into the shelter 30 minutes before the trial started. All trials were conducted in a room maintained at 28◦ C. To begin the trial, a focal Eulamprus was released into a glass tank (25 × 20 × 20 mm depth) containing a single shelter (130 × 130 × 20 mm depth) at one end. A video camera filmed the lizards’ behaviour from beneath, through the transparent floor of the enclosure. As soon as the Eulamprus was released into the centre of the arena, we encouraged it to move by tapping it on the tail with a paintbrush until it entered the shelter. The duration of time the Eulamprus remained within the shelter before fleeing was recorded for up to ten minutes, after which the time was recorded as ten minutes. The video also allowed us to describe behaviours of the lizards in more detail. For the focal Eulamprus inside the shelter we scored: (1) rate of breathing (as shown by lateral movements of the chest cavity, a reliable indicator of stress, Avery, 1993); and (2) frequency of subordinate behaviours (flee from shelter; reverse slowly out of the shelter; lash tail from side to side). Tail-lashing occurs in response to predator presence in many scincid species (Arnold, 1984; Torr & Shine, 1994; Cooper, 1998; Langkilde, 1999). We initiated behavioural observation of the focal Eulamprus once the Eulamprus entered the shelter. The numbers of breaths taken were counted for 20 seconds, and the subordinate behaviours were recorded throughout the trials. Data for these behaviours were converted to frequencies per minute for analysis with ANOVA, followed by Tukey posthoc tests. For the stimulus Egernia we recorded three behaviours, in each of two 2-second intervals (at a random time since the beginning of the encounter; and also, immediately prior to the Eulamprus fleeing): (1) whether or not the Egernia was moving; (2) whether or not its mouth was open; and
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(3) whether or not it bit the Eulamprus during this period. We used contingency-table analyses to compare behaviours performed by Egernia immediately prior to the Eulamprus fleeing, with those during the randomly selected time interval. In this way, we could evaluate whether or not the specific behaviours we recorded for Egernia tended to precede flight by Eulamprus. We adopted a stepwise approach for these analyses, first looking at whether or not Eulamprus were more likely to flee after biting occurred (this was tested only within the trials where the Egernia were in undivided shelters), then (after deleting these cases) whether Eulamprus were more likely to flee in response to the open-mouth display, and then (after deleting these cases also) whether Eulamprus were more likely to flee after movement by Egernia. No animals were injured during these trials. All data were analyzed using Statview 5.0 (SAS Institute Inc. 1998).
Results Shelter-site choice All Egernia remained under the hot shelter for the duration of the trials. None fled from the shelters after the introduction of Eulamprus, but the reverse situation (flight by Eulamprus) was common. The mean number of times that the focal Eulamprus were observed under the hot shelter differed among the experimental treatments (two-factor ANOVA with treatment and focal sex as the factors and number of times under the hot shelter as the dependent variable: treatment, F3,18 = 10.15, p < 0.0001; Figure 1a). Posthoc tests show that individuals spent less time under the hot shelter in the presence of Egernia (whether caged or unrestrained) than they did in the control treatment, and less time under the hot shelter in the presence of an unrestrained Egernia than they did in the scented treatment, but there was no difference in hot-shelter use between the scented and control treatments, or between the scented and the caged Egernia treatments. Male and female Eulamprus responded in similar ways to the treatments, with no overall difference between the sexes (F1,54 = 1.56, p = 0.23) and no significant interaction between focal sex and treatment (F3,54 = 0.76, p = 0.52).
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Figure 1. Behavioural responses of Eulamprus to four experimental treatments in which they were offered a choice between a cold shelter and a hot (and thus, preferred) one with or without cues (scent, caged presence, unrestrained, control) of a larger aggressive lizard species (Egernia). The graphs show (a) the number of times that Eulamprus were observed under the hot shelter, (b) the frequency of subordinate behaviours by Eulamprus (flee, reverse and tail lash), (c) the number of breaths per minute by Eulamprus, and (d) the number of minutes that Eulamprus spent under the hot shelter prior to fleeing. Values are presented as means ± SE. Values with the same symbol are not significantly different from one another.
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Latency and stimuli to flight Latencies for Eulamprus to enter the shelter did not differ significantly among treatments (F3,27 = 1.48, p = 0.24). Once inside the shelter, however, the Eulamprus performed subordinate behaviours (flee, reverse, taillash) more frequently in trials where the shelter also contained an unrestrained Egernia than in any other treatment (repeated-measures ANOVA with treatment as the factor and frequency of subordinate behaviours as the repeated dependent variable: F3,27 = 5.98, p = 0.003; posthoc p < 0.05; Figure 1b). Similarly, they breathed more rapidly inside undivided shelters containing Egernia (one-factor ANOVA with treatment as the factor and respiratory frequency as the dependent variable: F3,27 = 9.8, p = 0.002; posthoc tests show that Eulamprus breath more frequently when faced with Egernia in undivided shelters than in either the control or scent treatments; Figure 1c). The time Eulamprus remained in the shelter also differed among treatments (one-factor ANOVA with treatment as the factor and minutes until flight as the dependent variable: F3,27 = 19.57, p < 0.0001; posthoc tests show that Eulamprus stayed in an undivided shelters containing Egernia for significantly less time than in all the other treatments; Figure 1d). Significant differences were also apparent in the behaviours that we recorded for Egernia in the periods immediately before the Eulamprus exited the shelter compared to a random, earlier time period of the same duration. Unsurprisingly, bites often occurred immediately before the Eulamprus fled (this comparison was made within the trials where Egernia were in undivided shelters only, because biting was not possible in the other treatments: χ12 = 5, p = 0.03; Figure 2). Even after these cases were deleted, a significant difference was apparent in the incidence of open-mouth displays: these preceded Eulamprus flight more often than expected by chance (in both Egernia treatments: χ12 = 4.41, p = 0.03; Figure 2). Lastly, after deleting all cases where the Egernia either bit or opened its mouth, Eulamprus were more likely to flee if the Egernia moved (in both Egernia treatments: χ12 = 4.75, p = 0.03; Figure 2). Thus, flight by Eulamprus was stimulated by Egernia behaviour (movement, open-mouth display, and biting).
Discussion Although much simpler than the natural environment, our experimental arenas contained features important to Eulamprus heatwolei in the field in
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Figure 2. The percentage of Egernia that exhibited specific behaviours (bite, open mouth, move) in 2-second time periods either immediately before Eulamprus fled from the shelters, or at a random time earlier in the same trial during the period that the Eulamprus and Egenia were both under the shelter. If these behaviours by Egernia induce flight by Eulamprus, we expect that the behaviours will occur more frequently in the time period immediately prior to flight by the latter species. ∗ Signifies a significant difference in the frequency of behaviours immediately prior to flight versus at a random time point during the encounter.
Kanangra-Boyd (Langkilde et al., 2003). That is, available shelters differed in thermal regimes (and thus, hotter ones were actively selected) but those hotter shelters often contained (or, based on scent cues, had previously contained) individuals of a larger and aggressive lizard species. Under these circumstances we have observed frequent attack by Egernia, and frequent flight by Eulamprus, in both the laboratory and the field. The major result from our trials was that the presence of deposited Egernia scent played no significant role in avoidance of shelter-sites by Eulamprus. For example, scented crevices were used as frequently as control crevices, and subordinate behaviours were never elicited by deposited scent alone. Field observations support this result, as Eulamprus will use shelter-sites previously occupied by Egernia within 10 days of the Egernia being removed, but presumably still containing some scent cues (Langkilde & Shine, 2004). Instead, Eulamprus avoided crevices only if an Egernia was physically present, and especially if it was unrestrained within the shelter. Compared to the treatment with an Egernia within an undivided shelter, this treatment allowed the Egernia to physically interact with the Eulamprus, which may have played a role in the more intense flight responses induced by unrestrained Egernia than by any other treatment.
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The most intense stimulus from Egernia was to bite the Eulamprus; this occurred in many trials and invariably induced immediate flight (i.e., we never recorded biting without immediate flight). However, biting was not essential to cause the Eulamprus to vacate a crevice; open-mouth display (which often precedes biting in Egernia: pers. obs.) was also highly effective, as were more subtle whole-body movements by the larger lizard. Thus, the multiple sources of information provided by an Egernia within an undivided shelter (including visual, tactile, chemical, and perhaps auditory information) provided a reliable indication of risk and modified retreat-site occupancy by Eulamprus. Given that previous work has emphasized the role of chemosensory information for retreat-site selection in lizards, why were visual and behavioural cues more important in our own study? Either Eulamprus were unable to detect scent deposited by Egernia, or the Eulamprus did not use the information gained from this scent for shelter-site selection. The first option is unlikely, as previous work has demonstrated acute chemosensory perception within this guild of lizards (Bull et al., 2001; Head et al., 2002; O’Connor, 2003). If avoidance by the subordinate animal was related entirely to the size and not species of the resident lizard, recognition of species-specific chemical cues might be irrelevant. However, in other experiments we have found that that it is the species, and not body size, of the resident that is most important in displacing another lizard (Langkilde & Shine, unpubl.). Thus, species recognition may play a role, though probably not via scent. Instead, the answer may lie with the costs and benefits of reliance upon different kinds of information. Scincid lizards occur at high densities in Kanangra-Boyd (pers. obs.) and strong interference competition for retreat-sites occurs not only intraspecifically, but also between all species-pairs (Langkilde & Shine, 2004). Although these lizards maintain a core home-shelter, they typically use several retreat-sites in the course of their day-to-day activities (O’Connor & Shine, 2003) and hence, most shelter-sites in the area will contain scent cues from one or more individuals. Under these conditions, a lizard that relied upon deposited scent cues for retreat-site selection would frequently avoid crevices that were actually unoccupied, and hence miss an opportunity to exploit the advantages (thermally, and in terms of predator protection) afforded by these ‘better’ crevices. Analogously, previous work has shown that skinks (including E. heatwolei) do not avoid shelters containing scent from wide-ranging active foraging snakes, perhaps because this scent would persist long after the predator
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has vacated the area (Head et al., 2002). Conversely, visual cues provide instantaneous and reliable information about not only the presence of a potential aggressor, but also its probable behaviour (via open-mouth display, etc.). Given that bites by Egernia during our study never caused significant injury to Eulamprus (pers. obs.), the costs of avoiding an occupied high-quality shelter site may be higher than the costs of investigating that site (and thus, risking attack by another lizard). In summary, data from our study are consistent with the hypothesis that animals utilize the information that is most pertinent to making appropriate (fitness-enhancing) ‘decisions’ about habitat selection. Even in lineages with highly developed chemosensory abilities, such as scincid lizards, some situations may favour reliance upon alternative kinds of information. A priori, the abiotic conditions within rock crevices would seem to facilitate the use of deposited scent cues (because these will be protected from the elements and thus tend to persist longer) and militate against visual information (because of poor illumination). However, the persistence of scent in fact reduces its usefulness as a predictor of whether or not a lizard entering that crevice is likely to be attacked. Under these circumstances, the immediacy and high information content of visual cues, combined with direct scent cues, may favour reliance upon such signals in habitat-selection ‘decisions’.
Acknowledgements We thank K. Robert, S. Iglesias, J. Herbert, and I. Van Hazel for assistance in the field, and D. O’Connor for sharing his insights into the ecology of montane skinks. The research presented here adhered to the Guidelines for the Use of Animals in Research, the legal requirements of Australia, and the ethics guidelines for the University of Sydney, NSW: Protocol No. L04/7-2002/3/3593. Animal collection was authorized by NSW Scientific Purposes Permit B2449. Financial support was provided by the Australian Research Council (to R. Shine).
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