Fil: Kacoliris, Federico Pablo. División Herpetología. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata; ArgentinaFil: Guerrero, Emiliano. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata; ArgentinaFil: Molinari, Alejandro. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata; ArgentinaFil: Moyano, B.. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata; ArgentinaFil: Rafael, Alberto. División Herpetología. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata; Argentin

Guerrero, Emiliano

Kacoliris, Federico Pablo

Molinari, Alejandro

Moyano, B.

Rafael, Alberto

Naturalis

213HERPETOLOGICAL JOURNAL 19:  213–216,  2009Short NotesRun to shelter or bury into thesand? Factors affecting escapebehaviour decisions inArgentinian sand dune lizards(Liolaemus multimaculatus)Federico P. Kacoliris, E. Guerrero, A.Molinari, B. Moyano & A. RafaelSección Herpetología, Departamento de Vertebrados,Museo de La Plata, ArgentinaThe goal of this study was to assess the main factorsaffecting escape strategies (escaping or sand burying)in sand dune lizards (Liolaemus multimaculatus). Werecorded body size, substrate temperature, approachdistance and shelter distance in the field, and performedan enclosure experiment to test whether mimickedpredator types (aerial or terrestrial) affect escapebehaviour. The frequency of sand-burying behaviourincreased with distance to shelter (represented bypatches of bunch grass; logistic regression, P<0.001),which was the single significant predictor of the escapestrategy chosen. However, in enclosure experimentsthe escape strategies adopted by lizards did not dependon predator type (contingency tables, P=0.62).Key words: burying, escape strategy, predator typeCorrespondence: Federico P. Kacoliris, Sección Herpetología, Departamento de Vertebrados, Museo de La Plata, Paseo delBosque s/n, La Plata (CP1900), Buenos Aires, Argentina. E-mail: fedekacoliris@yahoo.com.arVegetation structure and the availability of shelter arekey factors that determine space use andmicrohabitat preference in lizards (Scott, 1976; Pianka,1986; Huey, 1991; Lagos et al., 1995; Attum & Eason,2006; Nemes et al., 2006). Small lizards are generally athigh risk of predation, resulting in a trade-off betweenavoiding predators and competitors on the one hand, andthe acquisition of food, mates and refuge sites undergiven microclimatic conditions on the other hand (McIvor& Odum, 1988; Rocha, 1995; Converse & Savidge, 2003;Attum & Eason, 2006). Taken together, the availability ofshelters has profound implications for the ecology andsurvival of small lizards (Howard et al., 2003).Research on predator–prey interactions and escapebehaviour in lizards has received much recent attention.Iguanian lizards are often useful subjects for these kindsof studies, because they have high site fidelity, are oftenat high risk of predation and exhibit several escape strate-gies (Huey et al., 1983, Galdino et al., 2006), whoseeffectiveness depends on habitat structure and/or preda-tor type (Schoener & Schoener, 1980).The sand dune lizard, Liolaemus multimaculatus(Duméril & Bibrón, 1837), is a small diurnal sand-dwellinglizard endemic to the pampean coasts of the provinces ofBuenos Aires and Río Negro in Argentina, and is catego-rized as vulnerable (Cei, 1993; Lavilla et al., 2000). Sanddune lizards are microhabitat specialists, preferring areaswith low vegetation cover and bunch grasses as shelters(Kacoliris et al., 2006, 2008). They are, furthermore, sit-and-wait predators, but with a large prey spectrum (Vega,1997, 2001). Males of sit-and-wait lizards are generally ter-ritorial, and for this reason differences in space usebetween sexes could exist (Cooper, 1994). With regards toescape behaviour in the presence of predators, two strat-egies exist: burying into the sand (Halloy et al., 1998) and/or escaping to shelters that consist of dense patches ofbunch grass (Spartina ciliata and Panicum racemosum;Chebez & Kacoliris, 2008). Possible predators in the studyarea are raptors (Caracara plancus and Milvagochimango), gulls (Larus dominicanus, Chroicocephalusmaculipennis), and terrestrial animals such as foxes(Pseudalopex gymnocercus), wild cats (Oncifelisgeoffroyi) and snakes (Philodryas patagoniensis andClelia rustica).The goal of this work was to assess the main factorsaffecting escape strategies displayed by sand dune liz-ards. We tested the hypotheses that 1) the number ofindividuals that display sand-burying behaviour in-creases when the distance to shelter also increases; 2)adult lizards shows a greater frequency of sand-buryingbehaviour than juveniles; and 3) when aerial predatorsattack, the number of individuals that display sand-bury-ing behaviour is greater than the number of individualsthat display run-to-shelter behaviour.The study site comprised a dune area located withinMar Chiquita Provincial Reserve (37º37´S, 57º16´W) inBuenos Aires Province, Argentina. Three different natu-ral habitat types occur in the area. Ecotone grasslands arepsammophytic on stable dune substrate, located betweencoastal dunes and pampas grasslands, with high and ho-mogeneously spread vegetation cover. Sand grasslandsare also psammophytic, but with low to medium vegeta-tion cover dominated by plant species adapted to highsalinity, a mobile substrate and low water availability.Interdunes are humid depressions with a mix ofgrasslands and hygrophytic plants. Sand grasslands andinterdunes are distributed as patches in a matrix of activedunes with a lack of vegetation (Cabrera, 1976). Intro-duced trees (Pinus sp. and Acacia sp.) also occur withinthe study site.Fieldwork was performed during January and Februaryof 2008 and 2009. Each survey began at 1100, correspond-ing to the daily activity peak for this species (Vega et al.,2000), and finished at 1600. Three observers searched forlizards using visual encounter surveys that encompassedall microhabitat types (Crump & Scott, 1994). We simu-lated encounters with terrestrial predators in free-rangingsand dune lizards, and with terrestrial and aerial predatorsin an enclosure experiment.214For free-ranging lizards, when an individual was found,the same observer (FK, wearing similar clothes) pursuedthe lizard, simulating a terrestrial predator. The followingdata were recorded: 1) approach distance, i.e. the distancebetween the observer and the lizard at which the escapebehaviour was triggered (AD; to the nearest 1 cm); 2) thelizard’s distance to the closest shelter (DCS; to the near-est 1 cm); 3) substrate temperature in the first locationwhere the lizard was observed (T, to the nearest 1 ºC); and4) escape strategy displayed: taking refuge in a shelter(run-to-shelter), or burying into the sand (sand-bury).After the mimicked predator attack we captured the indi-vidual and recorded its sex (based on external features;Cei, 1993), snout–vent length (SVL, to the nearest 0.05mm), and tail state (normal or autotomized/regenerated).Temperatures were recorded only during the 2008 season,whereas all the other independent variables were re-corded only during the 2009 season.For the experiment, we enclosed a 32 m2 (8 m × 4 m) sandfield with plastic fences up to 1m high, placing a largebunch of grass that represented the preferredmicrohabitat for shelter (Kacoliris et al., in press) 6 m awayfrom a starting point for the lizards. We captured adult liz-ards and kept them for one day in a terrarium foracclimatization. For data collection, lizards were put intothe enclosure before simulating a terrestrial or an aerialpredator attack. Terrestrial predators were simulated bythe same observer (FK, wearing similar clothes) crawlingin the lizard’s direction, whereas aerial predators weresimulated by a wooden bird model with a rope system thatallowed the model to move in all directions above the en-closure. We again recorded the escape strategydisplayed by each lizard (run-to-shelter or sand-bury).Data are presented as means ± SE. All tests were two-tailed, with a significance level of a=0.05. Because escapestrategy is a binary variable, its relation with other inde-pendent variables was assessed using logistic regressionmodels. A simple logistic regression was performed toevaluate the relation between substrate temperature andthe escape strategy, whereas a backward stepwise logis-tic regression was performed to test the relation betweenthe independent variables (AD, DCS, SEX, SVL, TAIL)and escape strategy. For the enclosure experiments, weused contingency tables to assess whether the escapestrategy depended on the type of predator.A total of 149 free-ranging lizards (90 females and 59males) were used for the experiment. While 88% (n=130)were normal-tailed, 12% (n=19) had autotomized/regener-ated tails; tail condition had no influence on escape strat-egy. A total of 124 (84%) of the lizards ran to shelters inour presence, whereas 25 (16%) buried into the sand (Ta-ble 1). Substrate temperature and escape behaviour wereuncorrelated with each other (P=0.135). Backwardstepwise logistic regression modelling of escape strategyidentified DCS (–2 log likelihood = 26.13, P<0.001) as itsonly predictor, while the other variables did not show sig-nificant correlations (P=0.05 in all cases; Table 2). Asshown in Figure 1, the frequency of sand-burying behav-iour increased with distance to the closest shelter.We experimented with 68 lizards in the enclosure. Ofthe 42 lizards used in simulations of terrestrial predators,22 (52%) displayed run-to-shelter behaviour, while 20(48%) displayed sand-burying behaviour. In the case ofaerial attacks (26 individuals tested), nine lizards (35%)displayed run-to-shelter, while 17 (65%) displayed sand-burying behaviour. The contingency table did not revealsignificant differences between the predator types (chi-square = 1.84; P=0.61; df=3), rejecting our hypothesis thatescape strategy depends on predator type.Escape behaviour by sand dune lizards depends onshelter availability and proximity. When close to a shelter(at distances less than 3 m), lizards prefer to run to the ref-uge rather than bury into the sand. As distances to theclosest shelter increase, the number of individuals thatuse sand-burying behaviour also rises. Overall, runningto shelters is the most common escape strategy dis-played, whereas sand burying is only used when sheltersare unavailable or out of reach. Overall, running to shel-ters seems the preferred strategy over sand burying whenfacing predators.When sand-buried, lizards are only positioned a fewmillimetres below the surface, and may be unearthed if apredator is able to determine their location. On the otherhand, shelters such as bunches of grass provide a densebarrier against large animals, but small lizards can enterthem easily, virtually disappearing from predators’ sightand reach. It is also common that lizards bury when insidethe bunch grass.Our results show that lizards do not modify their es-cape behaviour depending on temperature, which might,however, modify their levels of activity. Further studiesshould include the body temperature of individuals asTable 1. Main characteristics (mean ± SE) of theparameters approach distance (AD, in cm), distance tothe closest shelter (DCS, in cm), size of lizards (SVL, inmm) and substrate temperature (T, in degrees Celsius).Variables Mean±SE (n=149) RangeAD 210.99±257.51 0–1427.00DCS 1742.07±2020.26 0–5650.00SVL 53.84±6.01 27.00–67.70T 33.00±4.95 22.00–49.10Table 2. Scores (-2 log likelihood) and P values of thelogistic regression between escape behaviour used bylizards and explicative variables: ED (escape distance),DCS (distance to closer shelter), SVL (snout–ventlength), TAIL (tail status) and SEX.Variables Scores P valuesED 0.261 0.610DCS 26.134 0.000SVL 0.804 0.370TAIL 0.002 0.968SEX 0.053 0.819F.P.  Kacol i r is  et  a l .215well as temporal variables of predator escape (delay untillizards display behaviours and the behaviours’durations). The lack of correlation between size and sexand escape behaviour conforms with previousautoecological studies that also failed to find differencesin microhabitat use between these categories (Kacoliris etal., 2009).Our data do not support the idea that differential es-cape strategies are used depending on whether a predatoris aerial or terrestrial. We initially assumed that sand bury-ing was a more effective strategy against aerial predators.Terrestrial predators are more likely able to dig up a buriedlizard, which would be out of reach during an aerial pur-suit. On the other hand, sand burying could be aparsimonious behaviour for lizards because individualsdo not need to move away from their original positions.However, 65% of attacks with the aerial predator replicaresulted in sand-burying behaviour, and further experi-ments are required in order to accurately assess whetheran actual difference in lizard escape strategies exists be-tween terrestrial and aerial predators.Acknowledgements. We thank N. Areta, I. Berkunsky andJ. Williams for valuable comments and suggestions. Wealso thank R. Cañete, F. Tuñon, M. Buzato, J. Mangiarotti,C. Estavillo, G. Guaitoli and Magda for assistance in thefield. Field work was supported by funds from RuffordSmall Grants and International Reptile ConservationFoundation. FK is supported by the Consejo Nacional deInvestigaciones Científicas y Técnicas de Argentina.Organismo Provincial de Desarrollo Sostenible gave per-mits for work in the study area.REFERENCESAttum, O.A. & Eason, P.K. (2006). 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Run to shelter or bury into the sand? Factors affecting escape behaviour decisions in argentinian sand dune lizards (Liolaemus multimaculatus)

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