An Unusual Ecology Among Whiptails: the Case of Cnemidophorus Lacertoides from a Restinga Habitat in Southern Brazil

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An unusual ecology among whiptails: The case of cnemidophorus lacertoides from a restinga habitat in Southern Brazil

Article in Journal of Natural History · November 2011 DOI: 10.1080/00222933.2011.597523

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Journal of Natural History Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnah20 An unusual ecology among whiptails: the case of Cnemidophorus lacertoides from a restinga habitat in southern Brazil C.V. Ariani a b , V.A. Menezes a , D. Vrcibradic a c & C.F.D. Rocha a a Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, 20.550-013, Rio de Janeiro, RJ, Brazil b Department of Genetics, Univeristy of Cambridge, Downing Street, Cambridge, CB2 3EH, United Kingdom c Departamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro, 22290-240, Rio de Janeiro, RJ, Brazil Available online: 28 Sep 2011

To cite this article: C.V. Ariani, V.A. Menezes, D. Vrcibradic & C.F.D. Rocha (2011): An unusual ecology among whiptails: the case of Cnemidophorus lacertoides from a restinga habitat in southern Brazil, Journal of Natural History, 45:41-42, 2605-2625 To link to this article: http://dx.doi.org/10.1080/00222933.2011.597523

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An unusual ecology among whiptails: the case of Cnemidophorus lacertoides from a restinga habitat in southern Brazil C.V. Ariania,b*, V.A. Menezesa , D. Vrcibradica,c and C.F.D. Rochaa

aDepartamento de Ecologia, Universidade do Estado do Rio de Janeiro, 20.550-013, Rio de Janeiro, RJ, Brazil; bDepartment of Genetics, Univeristy of Cambridge, Downing Street, Cambridge, CB2 3EH, United Kingdom; cDepartamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro, 22290-240, Rio de Janeiro, RJ, Brazil

(Received 5 August 2010; ﬁnal version received 13 June 2011; printed 1 September 2011)

We studied the ecology of Cnemidophorus lacertoides at a restinga habitat in southern Brazil. Peak activity occurred between 12.00 and 15.00. The mean body temperature of active lizards (35.0 ± 2.9◦C) was relatively low compared with other whiptails and was significantly influenced by environmental temperatures. Mean snout–vent length and mean body mass of individuals were 56.5 mm and 4.4 g, respectively. Male and female C. lacertoides were not significantly different in body size. Cnemidophorus lacertoides consumed 12 types of prey, with ants and spiders being the most important items. Unexpectedly, lizards did not consume termites, which tend to be very important items in the diets of most whiptails. We conclude that the population of Cnemidophorus lacertoides we studied deviates from the typical whiptail ecology because many of its ecological features differ from those of most other cnemidophorines of similar size. Keywords: ecology; whiptail lizard; Cnemidophorus lacertoides; restinga habitat; southern Brazil

Introduction Many aspects of lizard ecology are phylogenetically conservative, with thermal biology and foraging mode being good examples. It has long been known that closely related species tend to be active at similar body temperatures (Bogert 1949). Likewise, foraging strategy tends to be very conservative within lizard families (e.g. Vitt and Price 1982; Cooper 1994) and is, in turn, strongly associated with thermal requirements (e.g. Bowker 1984; Bowker et al. 1986; Verwaijen and Van Damme 2007). Therefore, there is usually a strong association between body temperature and foraging mode (and their respective correlates such as hourly activity patterns and diet composition) within a given lizard species, genus or even family (Huey and Pianka 1981; Magnusson

Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 et al. 1985; Perry 1999; Cooper 2005). Teiids and lacertids, for instance, are typically active foragers that feed primarily on sedentary (e.g. larvae) or spatially clumped prey (e.g. termites), maintain high body temperatures, and remain active for a relatively shorter period of the day when compared with ambush foragers (Pianka et al. 1979; Magnusson et al. 1985; Pianka 1986).

*Corresponding author. Email: [email protected]

The New World Teiidae, together with the Old World Lacertidae, represent the archetypal active foragers among lizards (Pianka and Vitt 2003). Within teiids, the Teiinae constitute the most speciose, widespread and well-studied group, mainly owing to the species that were until recently united in the single genus Cnemidophorus (collec- tively known as whiptails). Ranging throughout most of the Americas, from temperate to warm tropical climates, whiptails are nevertheless all superficially similar in body plan, size and habits: they are basically small-sized (usually less than 100 mm in snout– vent length (SVL)), long-tailed, streamlined ground-dwellers. These traits tend to set them apart from members of the other teiine genera (i.e. Ameiva, Dicrodon, Kentropyx and Teius), which are normally larger than 100 mm in SVL and, in the case of most Kentropyx, semi-scansorial. Nevertheless, in spite of the overall similarity in morphol- ogy and ecology among its members, the genus Cnemidophorus has been demonstrated to be non-monophyletic, based on molecular studies (Reeder et al. 2002; Giugliano et al. 2006). Notably, the genera Ameiva and Kentropyx are apparently embedded within Cnemidophorus, and the North and Central American species (now allocated to the genus Aspidoscelis) are more distantly related to the South American species (i.e. the lemniscatus group of Wright (1993)), but the relationships among the latter are less clear (Reeder et al. 2002). Thus, whiptails of the former genus Cnemidophorus may be more appropriately considered as a morphotype (or ecomorph), as their mor- phological and ecological similarities may be the result of convergence or retention of plesiomorphic traits rather than shared ancestry. The close relationship between Ameiva, Kentropyx and Cnemidophorus (sensu lato) had been previously hypothe- sized by Presch (1974) and, indeed, those three genera are now known to constitute a monophyletic group that Reeder et al. (2002) referred to as “cnemidophorines”. The members of the Cnemidophorus lacertoides complex, which are restricted to southern South America (Cei 1993), are some of the least well known of the cnemidophorines. Although this species complex belongs to the South American cnemidophorine radiation, its phylogenetic relationships to other members of this group are unclear (Reeder et al. 2002). Most species of the lacertoides complex have relatively small geographic ranges (Cei 1993; Cabrera and Carreira 2009; Rezende-Pinto et al. 2009), with the exception of C. lacertoides, which is broadly distributed in southern Brazil, Uruguay and northern Argentina (Peters and Donoso-Barros 1970; Cei 1993). Nevertheless, limited information exists on the biology of this species (Aún and Martori 1996; Feltrim 2002). Recently, a population of C. lacertoides was discovered at a coastal sand-dune area on the island of Santa Catarina, southern Brazil, represent- ing the northernmost record for the species (Vrcibradic et al. 2004a; identification of the specimens was confirmed by Gabriel Skuk and Gustavo Scrocchi). In the present study we analyse some aspects of the ecology of this population, providing compar- isons between C. lacertoides and other cnemidophorine species. We specifically address

Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 the following questions:

• What is the activity period of C. lacertoides? • What are the microhabitats preferentially used by C. lacertoides in the study area? • What is the spectrum of body temperatures in activity and the mean activity temperature of C. lacertoides, and to what extent are they affected by environmental temperatures? • What is the diet composition of C. lacertoidesinthe study area? • Is there sexual dimorphism in this population? Journal of Natural History 2607

Materials and methods Study area The survey was conducted in Santa Catarina island, in Florianópolis Municipality, Santa Catarina State, southern Brazil. This is a relatively large (424.4 km2) continental island separated from the mainland by a channel only 0.5 km wide. The study area is a restinga habitat located among the Joaquina dunes (27◦3749.1S, 48◦2744.0W), an extensive dune ﬁeld located on the eastern coast of the island. Restingas are quaternary sandy strips that occur along most of the Brazilian coastline, and are char- acterized mainly by herbaceous and shrubby xerophyllous vegetation and poor soils (Suguio and Tessler 1984). These habitats originated from successive marine regres- sions which occurred during the Pleistocene and Holocene periods (e.g. Muehe 1983; Perrin 1984; Kindel and Garay 2002). The study site is located within the “wet low- lands”of the Joaquina restinga (Figure 1) and consists of a valley surrounded by sand dunes and covered with vegetation, in which plants of the families Asteraceae, Fabaceae, Bromeliaceae, Eriocaulaceae and Orchidaceae are common (Castellani et al. 1995; Ariani et al. 2004). Apart from C. lacertoides, three other lizard species were also recorded by us in the area: the scincid Mabuya dorsivitatta (Vrcibradic et al. 2004b), the liolaemid Liolaemus occipitalis and the large tupinambine teiid Tupinambis merianae (pers. obs.).

Collecting methods and analysis Fieldwork was conducted in the summer, during three days in December 2003, two in December 2004 and three in December 2005, always between 07.30 and 18.00 and under the same weather conditions – warm and sunny. Lizards were collected during the same month every year so as to minimise possible interannual variations in weather conditions. December is one the warmest months in the area, averaging 23◦Cintem- perature and 147.8 mm in rainfall (INMET (Instituto Nacional de Meteorologia) 2005). Sampling effort was basically the same for each year, with the same four persons actively searching for lizards throughout the day. The animals were captured using elastic rubber bands and glue-traps, with the latter being randomly left at potential microhabitats and frequently checked (at least every 20 minutes) for trapped lizards. Animals found caught in glue traps were promptly removed from them (by dissolving the glue with ether). For each lizard collected (and also for those that were sighted but escaped), the hour of its ﬁrst sighting and the type of microhabitat it was using were recorded. The proportional availability of microhabitat categories in the habitat was estimated by walking along straight-line transects, totalling approximately 700 m, and recording the microhabitat available at a point every 160 cm of distance walked. The frequencies

Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 of microhabitat types recorded at the 436 points sampled thus provided an estimate of microhabitat availability. The proportional use of different microhabitat categories by the lizards was compared with the estimated proportional availability of the same categories in the habitat using the Kolmogorov–Smirnov two-group test (Siegel 1956). Immediately after capture, the body (Tb), substrate (Ts)andair(Ta) temperatures (the latter at 1 cm above substrate) were measured to the nearest 0.2◦C, with quick- reading cloacal thermometers (body temperatures of individuals caught in glue traps were not measured). Whenever Ta was being measured, the thermometer’s bulb was shielded from solar radiation and wind to minimize their effect on the reading. Simple and multiple regression analyses (Zar 1999) were used to evaluate to what extent body 2608 C.V. Ariani et al. A

C Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011

Figure 1. (A, B) Restinga habitat where Cnemidophorus lacertoides occurs and (C) termite mound, at the Joaquina dunes, Florianópolis, southern Brazil. Journal of Natural History 2609

temperatures (Tb) were related to environmental temperatures (Ta and Ts). Differences in body temperatures between males and females were tested by one-way analysis of variance (ANOVA; Zar 1999). All collected lizards were euthanized with ether and weighed in the field (to the nearest 0.2 g) using a Pesola® spring balance. The snout–vent length (SVL), head width (HW), head length (HL), jaw length (JL, measured from snout to mouth rictus) and tail length (TL, measured from cloaca to the end of the tail) of each individual lizard were also measured using a digital calipers (to the nearest 0.1 mm). Regenerated tails were not considered for the analysis of tail length. Lizards were categorised as adults or juveniles based on the minimum size at maturity (43 mm SVL), reported by Aún and Martori (1996) for an Argentinian population of C. lacertoides. Sexual dimorphism in SVL and body mass were tested by ANOVA, and inter-sexual differences in head size (HW, HL and JL) and tail length were tested comparing males and females using analysis of covariance (ANCOVA), with SVL as covariate (Zar 1999). The frequency of tail breakage for the studied population was also estimated based on the proportion of individuals with regenerated portions of the tail (considered as evi- dence of previous autotomy); animals whose tails were broken or lost during capture were not considered. All lizards collected were fixed in 10% formalin, transferred to 70% alcohol and later dissected for verification of gender and for analysis of stomach contents. Prey items were identified, counted and measured in their greatest length and width (to the nearest 0.1 mm, with a vernier caliper). Unidentified arthropod remains were grouped in a separate category, and were considered only for volumetric analyses. The number and the total volume (in mm3) of prey per stomach and of each prey category were estimated. To estimate the volume of each prey item we used the ellipsoid formula (Dunham 1983):

V= 4/3π(L/2)(W/2)2,(1)

where V = volume, L = length and W = width. To determine the relative contribution of each prey category in the diet, we cal- culated the importance index for individual and pooled stomachs using the following equation:

I=F%+N%+V%/3, (2)

where F% is the percentage of occurrence (proportion of stomachs containing a given prey category), N% is the numeric percentage and V% is the volumetric percentage

Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 (see Howard et al. 1999). To evaluate whether there were signiﬁcant differences in diet composition (number of prey per stomach and mean volume of individual prey consumed) between sexes ANCOVA was performed, with head length as covariate. The relationship between three morphometric variables (SVL, JL and HW) of the lizards and the mean prey volume were tested using simple regression analysis. Since whiptails, in general, are known to feed heavily on termites (e.g. Pianka 1970; Vitt et al. 1993; Mesquita and Colli 2003a, b; Teixeira-Filho et al. 2003), transects were run with the speciﬁc goal of providing an estimate of density of termite mounds in the 2610 C.V. Ariani et al.

area. During those transects, all termite mounds found within 5 m to either side of an observer walking on a straight line were recorded. The total distance walked by the observer was 500 m, with 10 m of width, providing approximately 0.5 ha of transected area. For all statistical tests, the normality of the variables was tested and whenever data did not approach a normal distribution logarithmic transformations were made. Arithmetic means are presented ±1 standard deviation throughout the text.

Results Activity, microhabitat use and thermal ecology Overall, 40 individuals of C. lacertoides (all adults) were collected during the study (14 in 2003, 14 in 2004 and 12 in 2005). Cnemidophorus lacertoides started and ended its activity at around 8.30 and 15.30, respectively, thus remaining active for a period of approximately 7 hours. After 16.00 no lizards were observed active in the field. The peak activity of the species occurred between 12.00 and 15.00 (Figure 2). Cnemidophorus lacertoides used six microhabitat categories, being found most frequently under herbaceous vegetation (37.1%; n = 26), followed by open sand (17.1%; n = 12). The available microhabitats most frequently recorded at the area were open sand (32%; n = 148), herbaceous vegetation (26%; n = 120) and grass tuft (12%; n = 55) (Figure 3). There was a significant difference between the pattern of microhabitat use by C. lacertoides and the distribution of potential microhabitats available in the study area (Dmax = 0.778; p = 0.005). ◦ The mean body temperature in activity (Tb)ofC. lacertoides was 35.0 ± 2.9 C (range 28.8–39.4◦C; n = 35), and mean air and substrate temperatures were 30.3◦ ± 2.9◦C (range 25.8–37.0◦C; n = 35) and 33.3 ± 7.1◦C (range 23.9–50.0◦C; n = 35), respectively. Lizard body temperatures were positively and significantly correlated 2 with air and substrate temperatures (Ta: F 1, 33= 30.07; R = 0.48; p < 0.001; Ts: 2 F 1, 33 = 9.06; R = 0.22; p < 0.001) (Figure 4). A multiple regression analysis indicated that the interaction of these two environmental temperatures influenced the body tem- 2 perature of C. lacertoides (F 2, 32 = 15.46; R = 0.49; p < 0.001), but only Ta had a

10 Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 5 Frequency (%) Frequency

0 7:00- 8:00- 9:00- 10:00- 11:00- 12:00- 13:00- 14:00- 15:00- 16:00- 17:00- 8:00 9:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00 18:00 Time (h)

Figure 2. Activity pattern of the whiptail lizard Cnemidophorus lacertoides (n = 85) at the Joaquina dunes, Florianópolis, southern Brazil. Journal of Natural History 2611

40 35 30 25 20 15

Frequency (%) Frequency 10 5 0 HV OS IB LB SB BB FA TG TM

Microhabitats

Figure 3. Proportional use by Cnemidophorus lacertoides (dark bars) and estimated proportional availability (light bars) of different microhabitat categories at the Joaquina dunes, Florianópolis, southern Brazil. HV: herbaceous vegetation; OS: open sand; IB: interior of bush; LB: leaf litter at the border of bush; SB: open sand at the border of bush; BB: base of bromeliad; FA: ﬂooded area; TG: tuft of grass; TM: termite mound.

signiﬁcant effect on Tb (p < 0.001) after factoring out the effect of the other variable. ◦ There was no signiﬁcant difference in mean Tb between males (34.7 ± 2.9 C; range ◦ ◦ ◦ 28.8–38.4 C; n = 21) and females (35.8 ± 3.0 C; range 29.6–39.4 C; n = 13) (F 1, 33= 1.21; p = 0.280).

Sexual dimorphism and tail break frequency Mean snout–vent length of C. lacertoides at the Joaquina restinga was 56.3 ± 4.2 mm (range: 44.8–63.0 mm; n = 40) and mean body mass was 4.4 ± 1.1 g (range: 2.3–6.6 g; n = 40). Males and females did not differ signiﬁcantly in SVL or in body mass (Table 1). Mean HW, HL and JL were 8.6 ± 0.8 mm (range: 4.4–10.5 mm; n = 40), 14.6 ± 1.0 mm (range: 12.7–16.7 mm; n = 40) and 10.8 mm ± 1.2 (range: 9.2–14.4 mm; n = 40) respectively, and were proportionally larger for males than for females (Table 1). Mean tail length of C. lacertoides was 108.5 ± 10.3 mm (range: 91.6–124.9 mm; n = 26) and was greater (relative to SVL) for males than for females (Table 1). The frequency of tail breakage in our sample was 17% (6/35). Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 Diet Of the 40 individuals of C. lacertoides examined, two (a female from 2003 and a male from 2005) had empty stomachs. A total of 13 prey categories were identiﬁed in the stomachs of the remaining animals, with Formicidae and Araneae being the dominant items in the diet (Table 2). Most of the diet of C. lacertoides (91.8%) was composed of relatively mobile prey (mainly ants and spiders) compared to sedentary prey (e.g. larvae, mites and gastropoda). Mean prey volume was 199.1 ± 294.2 mm3 (range 0.2–1437.4mm3, n = 162), and mean number of prey items per stomach was 4.4 ± 3.6 2612 C.V. Ariani et al. Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011

Figure 4. Relationship between body temperature (in ◦C) of the lizard Cnemidophorus lacer- 2 toides and air temperature (F 1,33 = 30.07; R = 0.477; p < 0.001; n = 35) (top), and substrate 2 temperature (F 1,33 = 9.06; R = 0.215; p < 0.001; n = 35) (bottom), at the Joaquina dunes, Florianópolis, southern Brazil. Journal of Natural History 2613 13 13 = = n n 9.6 11.4 ± ± 22.548 0.001 = statistic probability < 24 at the restinga of the , = (93.8–121.6); (91.6–124.9); p 1 p 108.2 mm 108.9 mm F 18 22 = = n n 0.7 1.4 ± ± 37.39 sample size and 0.001 = = < 38 n , (9.2–12.2); (9.3–14.4); p 1 10.5 mm 11.0 mm F Cnemidophorus lacertoides 18 22 = = n n 0,8 1.1 ± ± 1.021 0.37 = = 37 , (12,7–15,8); (12.7–16.7); p 1 14.2 mm 14.9 mm F 22 18 = = n n 0.4 0.9 ± ± 13.3 –– –– 0.001 = < 37 , (7.4–8,9); (7.4–10.5); p 1 1 standard deviation (SD), range in parentheses, F 8.2 mm 8.8 mm ± 18 22 = = n n 0.092 1.1 1.1 0.763 = ± ± = 38 , (2.8–6.6); (2.3–6.4); p 1 4.4 g F 4.1g Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 18 22 = = n n 3.8 4.5 ± ± 1.926 0.17 = = 36 , (50.0–63.0); p (44.8–62.5); 1 F ANOVA Female 56.8 mm ANCOVA – – (signiﬁcant values shown in bold). Table 1. Means of(TL; the mm) snout–vent of length males (SVL; and mm), females, body and mass the (g), statistics head results width for (HW; the mm), sexual jaw differences length on (JL; these mm), variables, head for lengthSexes (HL; mm) and tail length Male SVL 55.9 mm Body mass HW JL HL TL Joaquina dunes, southern Brazil. Values represent means 2614 C.V. Ariani et al. X I % F 38) = 0.1) 18.4 7.9 0.1) 2.6 1.2 0.1) 2.6 1.0 n 0.1) 2.6 1.0 < < < (%) < V unidentiﬁed arthropod remains. = (%) N X I x). U.A.R. I % F 17) Total ( = n 0.1) 29.4 35.6 9 (5.5) 12.0 ( 0.1) 5.9 2.3 2 (1.2) 78.5 (0.4) 5.2 2.2 0.1) 5.9 2.3 1 (0.6) 9.4 ( (%) < < < V %) and importance index ( F (%) N at the Joaquina dunes, southern Brazil. The contribution of each prey category to the diet is X I ), frequency of ocurrence ( 3 % F 21) Females ( ;mm V = n 0.1) 9.5 4.7 6 (6.2) 8.0 ( (%) < Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 V Cnemidophorus lacertoides Males ( ), volume ( N (%) – – – – 1 (1.0) 37.9 (0.3) 5.9 2.4 1 (0.6) 37.9 (0.2) 2.6 1.1 – 1922.1 (23.9) 28.5 – – 3783.1 (33.8) 35.3 – 5705.2 (29.6) 31.6 65 8082.4 97 11213.4 162 19295.8 N 1 (1.5) 12.1 (0.1) 4.7 2.1 – – – – 1 (0.6) 12.1 ( 2 (3.0) 26.1 (0.3) 9.5 4.2 2 (2.0) 125.6 (1.1) 11.7 4.9 4 (2.4) 151.7 (0.8) 10.5 4.5 30 (46.1) 3776.9 (46.8) 52.4 48.4 41 (42.3) 4640.5 (41.5) 64.7 49.5 71 (44.0) 8417.4 (43.7) 57.8 48.5 AdultsLarvae 5 (8.0) 1 (1.5) 121.5 (1.5) 76.3 (0.9) 19.0 4.7 9.5 2.3 1 (1.0) 1 (1.0) 60.9 (0.5) 2.2 ( 5.9 2.4 6 (3.7) 182.4 (1.0) 13.1 5.9 Non- AdultLarvae 1 (1.5) – 66.8 (0.8) 4.7 – 2.3 – – – – 1 (1.0) 9.4 ( – – 1 (0.6) 66.8 (0.3) 2.6 1.1 AraneaeAcarina 17 (26.1) 1264.1 (15.7) 42.8 3 (4.6) 28.2 4.0 ( 39 (40.3) 1851.9 (16.6) 64.7 40.5 56 (34.7) 3116.0 (16.1) 52.6 34.5 Coleoptera Orthoptera 4 (6.2)BlattodeaIsoptera 768.2 (9.5)Hemiptera 1 (1.5) 19.0 43.8 (0.5) – – 11.5 4.7 3 (3.1) 2.2 – 681.2 – (6.0) 17.6 – – – 8.9 – 7 – (4.3) – 1449.4 (7.5) 2 (2.0) – 18.4 12.5 (0.1) – 10.1 – 5.9 – 1 (0.6) 2.6 2 (1.2) – 43.8 (0.2) 12.5 ( 2.6 – 1.1 – – Hymenoptera Diptera Arachnida Table 2. Diet composition of Prey Category Mollusca Gastropoda given in terms of number ( Hexapoda Formicidae Formicidae Lepidoptera (larvae) Total U.A.R. Journal of Natural History 2615

(range 1–18, n = 38). The mean total volume consumed per stomach was 890.5 ± 658.3 mm3 (range 23.4–2325.0 mm3; n = 38). No significant difference was detected between males and females in terms of total number of prey (log-transformed) per stomach 2 (F 1, 33= 3.14; R = 0.11; p= 0.06) or in mean prey volume ingested (log-transformed) 2 per individual (F 1, 33= 0.53; R = 0.03; p = 0.59). Mean prey volume (log-transformed) was not significantly related with either lizard jaw length (F 1, 34= 3.04; p = 0.09) or head width (F 1, 34= 0.42; p = 0.52), but was positive and significantly related to SVL 2 (F 1, 34= 5.57; R = 0.13; p = 0.02). Transects for estimates of density of termite mounds in the study area yielded a total count of 14 mounds, giving an estimated density of 28 termite mounds/ha. All termite mounds recorded were inhabited and the termites were always active (Figure 1).

Discussion Activity, microhabitat use and thermal biology Cnemidophorus lacertoides had a unimodal activity pattern in the area, with a peak during the afternoon (12.00 to 15.00), which is somewhat unusual among cnemidophorines. Table 3 summarises the peaks of activity of other cnemidophorine species from South America, suggesting that they tend to be active mostly during the morn- ing, unlike the studied population of C. lacertoides.Also,C. lacertoides remains active for a relatively long period (about seven hours) of the day, whereas most of the South American whiptail species studied so far tend to have a shorter activity period, usually about six hours or less (e.g. C. abaetensis – Dias and Rocha 2004; C. cryptus, C. gramivagus and C. parecis – Mesquita and Colli 2003a; C. littoralis – Teixeira-Filho et al. 1995; C. longicaudus – Villavicencio et al. 2007; C. nativo – Bergallo and Rocha 1993, Menezes et al. 2000; C. ocellifer – Vitt 1995, Menezes et al. 2011). Most of these species, like C. lacertoides, occupy open habitats (as expected for heliophilous lizards). Cnemidophorus lacertoides had a relatively low body temperature (mean = 35◦C) compared with other similar-sized South American cnemidophorine species, whose mean body temperatures are usually about 37–39◦C or higher (Table 3).The mean body temperature of C. lacertoides at the Joaquina restinga was more similar to those of Amazonian species of the cnemidophorine genus Kentropyx (Vitt and Carvalho 1992; Vitt et al. 1995, 1997b, 2001), which typically inhabit forested and/or riparian habitats, and thus tend to occur at more mesic conditions than most other South American teiines (including C. lacertoides). The relatively low Tb of C. lacertoides could result from the adjustment of this population to the local thermal environment (see Kiefer et al. 2005), as the body temperatures of C. lacertoides showed a strong positive rela-

Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 tionship with local environmental temperatures. Occurrence at relatively high latitudes may partly explain the relatively low body temperatures of C. lacertoides compared to other South American whiptail species. The liolaemid Liolaemus occipitalis studied by Bujes and Verrastro (2006), at a restinga habitat at about 30◦S in southern Brazil, had a lower mean body temperature in activity (30.9◦C) than the closely related con- gener L. lutzae (33.9◦C) from a lower latitude (23◦S) restinga habitat in south-eastern Brazil (Rocha 1995). The southern Chilean Liolaemus magellanicus, the world’s southernmost lizard species, has low mean body temperatures (27◦C) compared to other 2616 C.V. Ariani et al.

Table 3. Peak of activity and mean body temperature in activity (T b)ofvariousspeciesof whiptail lizards (Cnemidophorus) from different types of open habitat in South America. Values represent means ± 1 SD unless otherwise stated.

◦ Species Habitat Peak of activity Mean Tb ( C) Source

C. abaetensis NE Brazil 10:00h–11:00h 36.7 ± 1.7 Dias and Rocha (restinga) 2004 C. cryptus Amazonian 11:00h–12:00h 39.4 ± 1.9 Mesquita and savanna Colli 2003a C. gramivagus Amazonian 9:00h–10:00h 37.6 ± 2.3 Mesquita and savanna Colli 2003a C. jalapensis central Brazil – 37.0 ± 1.8 Colli et al. 2009 (cerrado) C. lacertoides southern Brazil 12:00h -15:00h 35.0 ± 2.9 present study (restinga) C. lemniscatus Amazonian 9:00h–13:00h 38.5 ± 1.8 Mesquita and savanna Colli 2003a C. littoralisa SE Brazil 9:30h–10:30h 38.7 ± 2.0 Teixeira-Filho (restinga) et al. 1995 C. littoralis SE Brazil 10:00h–11:00h 38.6 ± 2.2 Hatano et al. 2001 (restinga) C. longicaudus WArgentina 13:00h -14:00h 36.7 ± 2.2 Villavicencio et al. (montane 2007 steppe) C. mumbuca central Brazil – 36.9 ± 0.3b Colli et al. 2003 (cerrado) C. murinus Bonaire island – 38.5 ± 1.8 Schall and Dearing 1994 C. murinus Bonaire island 9:00h–12:00h 37.2 ± 0.2b Vitt et al. 2005 C. nativoa SE Brazil 9:00h–13:00h 37.6 ± 2.0 Bergallo and (restinga) Rocha 1993 C. nativo NE Brazil 10:00h–12:00h 39.0 ± 2.0 Menezes et al. (restinga) 2000 C. ocellifer NE Brazil 9:00h–14:00h 39.7 ± 0.2b Vitt 1995 (caatinga) C. ocellifer central Brazil 11:00h–14:00h 37.5 ± 2.3 Mesquita and (cerrado) Colli 2003a,b C. ocellifer NE Brazil 10:00h–11:00h 36.5 ± 1.8 Dias and Rocha (restinga) 2004 C. ocellifer NE Brazil 10:00h–14:00h 37.6 ± 1.6 Menezes et al. (caatinga-rocky 2011 ﬁelds transition) Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 C. parecis central Brazil 10:00h–12:00h 38.2 ± 2.2 Mesquita and (cerrado) Colli 2003a

Notes: a -asC. ocellifer. b -mean± 1SE. Journal of Natural History 2617

congeners (Jaksic and Schwenk 1983). Among populations of the North American cnemidophorine Aspidoscelis tigris, mean body temperatures show a clinal pattern, decreasing with latitude (Pianka 1970). Such variations in mean activity body temperatures might be a consequence of distinct responses to latitudinal occurrence of these lizards and to the differences in the local thermal environment. It is also worth men- tioning that the restinga at the Joaquina dunes is often subjected to windy conditions during the day (pers. obs.), which could impose thermal constraints on the lizards and delay the onset of their activity (i.e. it would take longer for the local environment to warm up). However, as we do not have quantitative data on such weather conditions, there is no way to know to what extent the wind in the area may affect the thermal relations of the local C. lacertoides population, and be responsible for its low body temperature and relatively late peak of activity. Further studies should investigate whether the C. lacertoides lineage has evolved a physiological adaptation to lower body temperatures which may have enabled it to colonise higher latitudes and to increase the extent of its daily activity.

Sexual dimorphism and frequency of tail loss Our data indicate that male and female C. lacertoides from Joaquina were not significantly different in body size (SVL and mass), though males had proportionally bigger heads and longer tails. The same trends were reported by Feltrim (2002) for a pooled sample of C. lacertoides from several localities in Argentina, Uruguay and southern Brazil (Rio Grande do Sul State). On the other hand, females were the larger sex in a population of C. lacertoides from Rio Grande do Sul State studied by Balestrin et al. (2010), and Rezende-Pinto et al. (2009) observed the same trend in C. vacariensis (another species of the lacertoides group), although relative head size was greater for males in both cases. Among cnemidophorines, males tend to be larger than females both in body size and in relative head size (Anderson and Vitt 1990; Vitt and Carvalho 1992; Vitt et al. 1993, 2001; Ramirez-Bautista et al. 2000; Baird et al. 2003; Mesquita and Colli 2003a,b). This is probably a plesiomorphic trait for cnemidophorines (and for teiids in general), with the absent or inverse sexual size dimorphism in the C. lacertoides group being apparently a derived condition. Nevertheless, the proportionally larger heads of males in species of that group conforms to the typical teiid pattern. Large head size in cnemidophorine males is thought to be related to sexual selection, by accruing advantages during male–male agonistic interactions (Anderson and Vitt 1990). This may also be the case for C. lacertoides, though we did not witness intraspecific agonistic interactions during our fieldwork. We found a relatively low frequency of tail autotomy (17%) in this population,

Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 compared with other Neotropical teiids for which autotomy rates have been estimated (see Van Sluys et al. 2002). The low frequency of tail autotomy recorded for C. lacertoides in this study may indicate that this strategy of defense is not used very frequently by this population, or that the density of predators in the studied area is relatively low (see Cooper et al. 2004). Although we cannot assess predator pressure for lizards in the area, we have recorded the presence of some potential predators, including birds (egrets, hawks, burrowing owls), the large-bodied lizard Tupinambis merianae and the snake Philodryas patagoniensis, which is known to prey on lizards in other restinga habitats (Rocha and Vrcibradic 1998; Ariani et al. 2006). 2618 C.V. Ariani et al.

Diet The diet of Cnemidophorus lacertoides at the restinga of the Joaquina dunes was composed strictly of small invertebrates, with no consumption of plant material being observed. Insular lizard populations usually consume higher amounts of plant material than continental populations, mainly because arthropod availability tends to be lower on islands than in continental areas due to isolation and space constraints (Cooper and Vitt 2002; Olesen and Valido 2003). However, those trends were not found for the studied population of C. lacertoides, possibly on account of the large size of Santa Catarina island (424 km), its proximity to the mainland (only about 0.5 km at the nearest point), and the relatively recent split of the island from the continent (Maack 2001). Unexpectedly, no termites were recorded in the diet of the studied population of Cnemidophorus lacertoides. Instead, this species fed mainly on ants and spiders. Transects in the area confirmed the presence of termite mounds, which indicates that the lack of termites in that lizard’s diet is not due to the local absence of these insects. Termites are usually among the most frequent and important prey in the diet of most species of small-sized cnemidophorines and other teiines, both in South America (including a population of C. lacertoides from Argentina; see Table 4), and in Central and North America (e.g. Pianka 1970; Paulissen et al. 1988; Vitt et al. 1993). From 23 different populations listed on Table 4, just two (Cnemidophorus lemniscatus from Curuá-Una, northern Brazil and C. nigricolor from Los Rocques island, Venezuela) did not consume isopterans, and the frequency of occurrence of termites in the diet was higher than 50% in 10 populations. Ants do not tend to be favoured as food by teiines: besides C. lacertoides from Joaquina, just one other population in Table 4 (C. lemniscatus from Alter do Chão, northern Brazil) had a frequency of ant consumption higher than 40%. Isopterans represented more than 10% of the total food volume in the diet of 13 populations, whereas just one population – curiously, C. lacertoides from Córdoba, Argentina – had more than 10% of the total volume of its diet represented by Formicidae. These insects represented more than 40% of the total prey volume consumed by C. lacertoides at the Joaquina dunes. It is thus clear that teiines, and particularly cnemidophorines, tend to consume termites more frequently and in higher quantity than ants, but C. lacertoides may represent an exception within the group. We conclude that the population of Cnemidophorus lacertoides from the Joaquina restinga deviates from the typical whiptail ecology because its activity patterns, body temperature in activity and diet composition differ from those of most other cnemidophorines of similar size studied so far. Nevertheless, the studied population of C. lacertoides may occur at or close to the northern limit of the species’ range, and thus it is possible that some of the ecological peculiarities observed may reflect local Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 adaptations to a marginal habitat. Data on other populations of C. lacertoides across the species’ wide geographic range are needed, to assess whether the ecological traits observed in the present study are characteristic of the species as a whole or of just that particular population. However, as the present study was carried out only in December over three consecutive years, we believe that additional studies done in different sea- sons within a year at the same site are necessary in order to confirm our current findings (especially with regard to the apparent non-consumption of termites by the studied population). Journal of Natural History 2619 ) Continued ( 2007 2000 1996 et al. 2003 2006 Teixeira-Filho c 100mm. Percentages are given as 0.1 0.1 Zaluar and Rocha 0.1 Menezes et al. 13.0 Aún and Martori (%) ants Source ≤ < ∼ < V c (%) ants F populations of teiines with SVL / 9.0 ? ∼ (%) termites V ) in each case. V ? 0 0 17.6 0.4 Vitt et al. 1997a 31.1 11.6 27.8 3.8 Vitt et al. 1997a 22.238.2 1.5 22.5 16.7 17.7 0.9 0.6 Vitt et al. 1997a Colli et al. 2009 21.0 5.0 9.0 0.2 Dias and Rocha 15.9 4.1 43.2 4.8 Vitt et al. 1997a 55.0 30.0 5.0 86.792.8 31.0 69.7 6.7 7.2 1.0 Araujo 1991 68.0 10.8 9.0 (%) termites F Brazil Brazil Brazil Tocantins, central Brazil NE Brazil Brazil SE Brazil SE Brazil SE Brazil Argentina Brazil Locality Córdoba, ) and as volumetric proportions ( F Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 b 17 Curuá-Una, N 32 90 Boa Vista, N 1834 Rio Xingu, N Ponte Alta do 3844 Joaquina, S Brazil Alter do Chão, N 0 0 57.8 43.7 this study 69 Barra de Maricá, N 34 Dunas do Abaeté, 21 Barra de Maricá, 31 Jurubatiba, SE 30 Barra de Maricá, a abaetensis (juveniles) C. lemniscatus C. littoralis C. cryptus C. jalapensis C. lacertoides C. lemniscatus Cnemidophorus C. littoralis C. lacertoides C. lemniscatus frequencies of occurrence ( Table 4. Percentages (%) of termites and ants in the dietsSpecies of different species Ameiva ameiva C. littoralis 2620 C.V. Ariani et al. 2003b 2005 1994 Paulissen and Walker Tedesco et al. 1995 c c 2.0 Aún and Martori 1996 7.0 5.0 Colli et al. 2003 1.0 (%) ants Source ∼ ∼ < < V c c (%) ants F 8.0 ? 15.0 20.0 ∼ ∼ (%) termites V 0 0 35.0 ? 71.3 38.4 10.9 0.4 Menezes et al. 2008 47.071.9 21.0 21.566.0 10.0 9.4 13.9 4.0 1.9 4.8 Dias and Rocha 2007 Menezes et al. 2011 0.2 Capellari et al. 2007 28.3 14.9 ? 100 (%) termites F Brazil island, Venezuela NE Brazil Argentina Brazil NE Brazil Argentina Brazil Locality Central Brazil 54.5Córdoba, 44.3 11.4 0.9 Mesquita and Colli Downloaded by [University of Cambridge], [Cristina Ariani] at 00:56 28 September 2011 b b 20 Grand Rocques 40 Dunas do Abaeté, 3251 Morro do Chapéu, 30 Monte Quemado, 42 Guriri, SE Brazil 51.1 ? 17 ? Teixeira 2001 21 Dom Feliciano, S 101 Guaratiba, NE N 166 Mateiros, central 202 C. ocellifer. -as a sp. n. 83 Ibiraba, NE Brazil 0 0 27.7 3.2 Rocha and Rodrigues - sample contains individuals from several different localities. - values represent Hymenoptera as a whole and, thus, may be overestimated. (juveniles) C. nativo C. nativo C. nigricolor Table 4. (Continued). Species C. mumbuca Notes: b c C. ocellifer C. Teius oculatus C. ocellifer C. serranus C. ocellifer C. ocellifer Journal of Natural History 2621

Acknowledgements This study is a portion of the results of the Eastern Brazilian Vertebrate Ecology Project (Laboratory of Vertebrate Ecology), of the Departamento de Ecologia, Instituto de Biologia, Universidade do Estado do Rio de Janeiro. Permission to collect the lizards was conceded by the Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis - IBAMA. We thank the Instituto Biomas for logistical support. This study was partially supported by research grants from the Conselho Nacional do Desenvolvimento Cientíﬁco e Tecnológico (CNPq) (processes # (307 653/2003-0 and 476684/2008-8). CVA received a graduate grant from FAPERJ and VAM a graduate grant from CNPq. Currently VAM is associated to the Programa de Pós-Graduação em Ecologia from Universidade do Estado do Rio de Janeiro and receives a Post-Doctoral grant from FAPERJ. CFD Rocha received research grants from the Conselho Nacional de Desenvolvimento Cientíﬁco e Tecnológico (CNPq) (processes 304791/2010-5 and 470265/2010-8) and from the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) through the “Cientistas do Nosso Estado” Program (process E-26/102.404.2009). CVA is currently a PhD student at the University of Cambridge and is sponsored by the Cambridge Overseas Trust.

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