Sexual Dimorphism and Natural History of the Western Mexico Whiptail, Aspidoscelis Costata (Squamata: Teiidae), from Isla Isabel, Nayarit, Mexico

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NORTH-WESTERN JOURNAL OF ZOOLOGY 10 (2): 374-381 ©NwjZ, Oradea, Romania, 2014 Article No.: 141506 http://biozoojournals.ro/nwjz/index.html

Sexual dimorphism and natural history of the Western Mexico Whiptail, Aspidoscelis costata (Squamata: Teiidae), from Isla Isabel, Nayarit, Mexico

Raciel CRUZ-ELIZALDE1, Aurelio RAMÍREZ-BAUTISTA1, *, Uriel HERNÁNDEZ-SALINAS1,2, Cynthia SOSA-VARGAS3, Jerry D. JOHNSON4 and Vicente MATA-SILVA4

1. Centro de Investigaciones Biológicas (CIB), Universidad Autónoma del Estado de Hidalgo, Carretera Pachuca-Tulancingo, Km 4.5 s/n, Colonia Carboneras, Mineral de La Reforma, A.P. 1-69 Plaza Juárez, C.P. 42001, Hidalgo, México. 2. Instituto Politécnico Nacional, CIIDIR Unidad Durango, Sigma 119, Fraccionamiento 20 de Noviembre II, Durango, Durango 34220, México. 3. Laboratorio de Herpetología, Escuela de Biología, Benemérita Universidad Autónoma de Puebla, C. U. Boulevard Valsequillo y Av. San Claudio, Edif. 76, CP. 72570, Puebla, Puebla, México. 4. Department of Biological Sciences, University of Texas at El Paso, 500 West University Avenue, El Paso, TX 79968, USA. *Corresponding author, A. Ramírez-Bautista, E-mail: [email protected]

Received: 25. April 2014 / Accepted: 13. June 2014 / Available online: 16. October 2014 / Printed: December 2014

Abstract. Lizard populations found in insular environments may show ecological and morphological characteristics that differ from those living in continents, as a result of different ecological and evolutionary processes. In this study, we analyzed sexual dimorphism, reproduction, and diet in a population of the whiptail lizard, Aspidoscelis costata, from Isla Isabel, Nayarit, Mexico, sampled in 1977 and 1981. Males and females from Isla Isabel showed no sexual dimorphism in many morphological structures, such as snout-vent length (SVL), but they did in femur length (FL) and tibia length (TL). Both sexes displayed synchronous reproductive cycles. However, males had smaller SVL (47.0 mm) in average than females (59.0 mm) at sexual maturity. The average clutch size was 2.4 eggs, but there was no correlation between egg number and female’s SVL. The diet of A. costata consisted of insects, arachnids, crustaceans, and plant material. Insects were the most consumed prey item, being mostly represented by orthopterans, coleopterans, and hymenopterans. Diet breadth of males was higher (Levin´s formula, B = 0.596) than in females (B = 0.358),

and diet overlap between sexes was relatively high (Pianka’s index, Ojk = 0.822), with an overlap ranging from 66.2 to 100%. The population of A. costata from Isla Isabel shows different morphological and ecological characteristics from their continental counterparts, but future studies on whiptail species with island and mainland populations are required to determine the ecological and evolutionary patterns.

Key words: Aspidoscelis costata, clutch size, diet, Isla Isabel, Mexico, Teiidae.

Introduction phism (SSD), in the form of anatomical differences between the sexes, has evolved due to an advan- Several ecological and evolutionary studies in- tage for larger males being selected by females, volving reproduction, diet, and sexual dimor- because large body size increases survival prob- phism conducted on island vertebrates (mammals, ability, which can be passed on to offspring birds, and reptiles) have generated great interest (Anderson & Vitt 1990, Butler et al. 2000), and 2) in the scientific community (Boback 2003, Lo- Niche divergence, which assumes that such sexual molino 2005, Meiri 2008), particularly with regard differences have evolved due to intraspecific niche to adaptive processes of life on islands (Channell divergence in nutritional requirements, or selec- & Lomolino 2000, Lomolino et al. 2006). Evolu- tion for different habitats (Stamps 1983, Shine tionary processes including morphological (e.g., 1989, Hierlihy et al. 2013). sexual dimorphism) and ecological characteristics Several studies have tested some life-history (e.g., differentiation in diet, clutch size, and snout– characteristics of populations found in insular en- vent length [SVL] at birth) are well documented in vironments. For example, Andrews (1979) found vertebrates inhabiting islands (Lomolino et al. high sexual dimorphism in lizard populations of 2006). Sexual dimorphism and diet preference are the genus Anolis, with sexual dimorphism biased central components for understanding life-history to males and mainly caused by competition for evolution of lizard species inhabiting islands (An- food resources and territory. On the other hand, drews 1979, Meiri 2008). Hasegawa (1994, 1997) found that some lizards in- With respect to lizards, sexual dimorphism habiting islands had larger males due to diet type, can be explained by two hypotheses: 1) Sexual se- as larger body and head sizes were required to fa- lection, which assumes that sexual size dimor- cilitate, with the aid of bacteria, the consumption Sexual dimorphism and natural history of the whiptail lizard 375 and digestion of cellulose associated with their hindlimbs), forearm length (FL: ± 0.1 mm; length from the vegetarian diets. Herbivory in island lizards has elbow to the pad of the foot), head width (HW: ± 0.1 mm; been associated with high availability of fruits maximum width of the head, measured as the distance between the posterior margin of the left and right ears), (Olensen & Valido 2003). Therefore, island lizards head height (HH: ± 0.1 mm; length of the earpiece open- may evolve sexual dimorphism in morphological ing height), head length (HL: ± 0.1 mm; length from tip of characters, while developing dietary differences snout to the posterior margin of the tympanic mem- between sexes, as reported for some birds (Grant brane), femur length (FEL: ± 0.1 mm; distance from the 1965). angle of the groin to the knee), and tibia length (TL: ± 0.1 The genus Aspidoscelis is one of the most di- mm; length from the knee to the pad of the foot; Olsson et verse genera in North America, including Mexico, al. 2002, Aguilar-Moreno et al. 2010). These morphological characters were measured to the nearest 0.1 mm. Be- where 43 species are currently recognized (Reeder cause these variables usually vary with SVL, we first cal- et al. 2002, Wilson et al. 2013). Species in this ge- culated regressions of log10-transformed data for all vari- nus are found in many environments, both in is- ables with log10-transformed SVL (Schulte-Hostedde et al. lands and on the mainland. However, few studies 2005). For significant regressions, we calculated residuals have evaluated the different biological aspects of from the relationship of variables on SVL to produce SVL- populations living in continental or oceanic is- adjusted variables. We used these residuals to examine lands. Currently, little information is available on sexual size differences between males and females and performed a Mann-Whitney U-test (Ramírez-Bautista & the natural history of Aspidoscelis costata (Teiidae), Pavón 2009, Ramírez-Bautista et al. 2013). The normality a species known from both the mainland and ad- of the data was verified by the Kolmogorov-Smirnov test jacent islands on the Pacific. Herein, we evaluate and Lillifors probability. We calculated a Pearson’s prod- sexual dimorphism in body size, aspects of diet, uct-moment correlations coefficient to test for relationship and reproduction of a population from Isla Isabel, between the morphological characters and the prey size Nayarit, Mexico. of males and females. The data are presented as mean ± SE, unless otherwise indicated. Reproductive characteristics. The following linear Material and methods measurements were taken to the nearest 0.1 mm on ne- cropsied lizards: SVL, length and width of right testis in Study area adult males; length and width of right and left nonvitel- This study was conducted in Isla Isabel (21° 52´ 30´´ N, logenic follicles (NVF), vitellogenic follicles (VF), and the 105° 54´54´´ W; datum: WGS84). The dominant vegetation number of ovulated eggs in adult females (Ramírez- type on the island is tropical dry forest, and the climate Bautista et al. 2000, Ramírez-Bautista & Pardo-De la Rosa has been described as tropical sub-humid with summer 2002). Additionally, the number of NVF and VF in ovaries rains (García 1973). The minimum ambient temperature and oviductal eggs in each oviduct was also recorded. has been reported as 22.6°C in January and a maximum of The length and width of gonads were used to obtain 30.3°C in September (CONANP 2005). testicular and follicular volume (V), calculated with the formula for the volume of an ellipsoid: V = 4/3 πa2b, Sampling where a is one-half the shortest diameter and b is half the A total of 121 lizards (78 males, 43 females) were captured longest diameter (Selby 1965). Testicular and follicular in April 1977 (n = 43) and May 1981 (n = 78). Both sam- volumes were used as indicators of reproductive activity ples were acquired during the spring, when the reproduc- in male and female lizards, respectively (Ramírez- tive activity of males (sperm production) and females Bautista et al. 2000, Ramírez-Bautista & Pardo-De la Rosa (vitellogenic follicles and eggs production) were at their 2002). The difference in testicular and follicular volume maximum. All specimens were euthanized in the labora- between the April and May collections was tested with a tory by lowering body temperature and fixed with a 10% Mann-Whitney U-test (z). The smallest adult female (SVL formalin solution using the methods described by = 59.0 mm) containing enlarged vitellogenic follicles or Ramírez-Bautista et al. (2000), and deposited in the herpe- oviductal eggs was used to estimate the minimum SVL at tological collection of the Centro de Investigaciones sexual maturity (Vitt & Cooper 1985, Ramírez-Bautista et Biológicas (CIB), Universidad Autónoma del Estado de al. 2000, Ramírez-Bautista & Pardo-De la Rosa 2002). The Hidalgo. minimum size of adult males at sexual maturity (SVL = 47.4 mm) was based on the size of the smallest male con- Data analysis taining enlarged and highly convoluted epididymides Sexual dimorphism. All data on morphological descrip- (Lozano et al. 2014). Therefore, individual females and tions and comparisons used to determine sexual dimor- males with a SVL < 59.0 and 47.4 mm, respectively, were phism were taken from adults of both sexes, as were data considered as juveniles. Clutch size was determined by on reproductive characteristics. For all lizards collected, counting the number of eggs in the oviducts and the vitel- we measured snout-vent length (SVL: ± 0.1 mm), interax- logenic follicles in the ovaries. A comparison between the ial width (IW: ± 0.1 mm; distance between forelimbs and number of oviductal eggs and vitellogenic follicles was 376 R. Cruz-Elizalde et al. tested for accuracy by using a Mann-Whitney U-test to was 67.9 + 1.1 mm (range 47.4 – 88.0), and of fe- determine clutch size. We calculated a Pearson’s product- males (n = 35) was 67.6 + 0.8 mm (59.0 – 78.1). moment correlation coefficient to test for a relationship There was no sexual dimorphism in SVL, IW, HW, between clutch size and female SVL. Liver and fat bodies HH, HL, and FEL. However, differences were ob- were removed and weighed to the nearest ± 0.0001 g on a scale. Liver mass and fat body mass were tested for a dif- served in FL and TL (Table 1). ference between males and females using a student t-test (t). A Pearson’s correlation was used to test for a relation- Reproductive characteristics ship between liver mass and fat-body mass to SVL in both The smallest mature male had a SVL of 47.4 mm sexes. A regression analysis was performed to know the with a testis volume of 9.5 mm3 (Table 2). The tes- influence of both liver mass and fat body mass on clutch ticular volume was higher in April (mean = 32.2 + size. 2.5 mm3; 8.6 – 53.9; n = 25) than in May (mean = Because organ mass or volume varies with SVL, we 23.3 + 2.7 mm3; 0.9 – 82.0; n = 48; z = -2.99, P = first calculated regressions of log10-transformed organ volume data against log10 of female and males SVL 0.003). The minimum SVL at sexual maturity for (Ramírez-Bautista & Vitt 1997). For regressions that were females was 59.0 mm. The mean number of vitel- significant, we calculated residuals from the relationship logenic follicles was similar (2.9 + 0.2; n = 19) to of organ volume to SVL. oviductal eggs (2.4 + 0.4; n = 5; z = -1.10, P = Feeding characteristics. The stomach contents of 0.271). The mean egg volume and mass were adults (n = 103) and juveniles (n = 13) were collected and 1133.0 + 110.3 mm3 and 1.6 + 0.3 g, respectively. identified to the level of taxonomic order. Because no statistical differences, determined by a student t-test (t), Different classes of ovocytes were present in adult were observed between stomach contents of adults females with different SVL. For example, the (males, n = 69; females, n = 34) and juveniles (males, n = smallest females (mean SVL = 65.9 + 2.0 mm; n = 4; females, n = 9), both age classes were pooled into their 6) exhibited NVF, the larger females (mean SVL = respective sexes for evaluation. The stomachs of five adult 67.2 + 1.0 mm; n = 19) displayed VF, and the larg- males were empty and were excluded from further analy- est females (mean SVL = 71.6 + 2.1 mm; n = 5) con- ses. The stomach contents (S = number of stomachs with tained oviductal eggs. There was no significant re- item i) were examined under a stereomicroscope to iden- tify individual prey items (n = number of prey items), and lationship between clutch size (vitellogenic folli- to calculate the percentage of stomachs with item i (%S). cles and oviductal eggs combined) and female’s The volume of food items (V) of each prey category in a SVL (r = 0.008, P = 0.892). single stomach was determined by using the formula: V = Liver mass in males was lower (mean = 0.20 + length x width x height (Acosta 1982), thereby establish- 0.01 g, 0.04 – 0.42; n = 73) than in females (mean = ing both the volumetric proportion (V) and the numerical 0.22 + 0.01 g, 0.06 – 0.45, n = 35; t = 2.823, P = percentage of total volume (%V) represented for each 0.006). However, fat-body mass was similar (t = food item (Vitt & Ohmart 1975). A student t-test (t) was used to test for a difference in the volume of prey items 0.887, P = 0.377) between males (mean = 0.05 + between males and females. 0.01 g, 0.02 – 0.53) and females (mean = 0.07 + 0.02 We calculated the Importance Value (ViI; Acosta g, 0.002 – 0.47). There was a significant relation- 1982) of each prey item eaten by males and females with ship between male’s SVL and fat-body mass (R2 = the formula: ViI = P’i + A’i + C’i; where ViI = importance 0.120, F1, 72 = 17.3, P < 0.001), and liver mass (R2 = value of the taxon i, P’i = Pi/∑Pi (Pi = total mass of the 0.69, F1, 72 = 154.4, P < 0.001). A similar pattern oc- taxon i; ∑Pi = total mass of all taxa), A’i = Ai/∑Ai (Ai = curred for liver mass (R2 = 0.34, F1, 34 = 17.6, P = number of prey that belong to taxon i; ∑Ai = total number of prey), C’i = Ci/∑Ci (Ci = number of stomachs that con- 0.0002) and female SVL, but not for fat-body mass tained taxon i; ∑Ci = total number of stomachs). and female SVL (R2 = 0.004, F1, 33 = 0.122, P = We calculated niche breadth using Levin’s (1970) 0.729). A regression analysis showed that clutch formula (B = 1/∑Pj²). We calculated niche overlap be- size was not related with fat-body mass (R2 = 0.23, tween females and males using Pianka’s (1986) index (Ojk F1, 4 = 0.88, P = 0.418) or liver mass (R2 = 0.71, F1, 4 = n n 2 n 2 = ∑i PijPik / ∑i Pi j ∑i Pi k). The breadth of the diet and 7.23, P = 0.075). diet overlap was determined for males, females, and juveniles by using the software program in Ecological Methodology (v. 6.1.1; Krebs 1999). Feeding characteristics The mean number of prey items consumed from April 1977 and May 1981 by males (1.34 + 0.13, 1– Results 14) and by females (2.14 + 0.35, 1–17) was different (t = 2.396, P = 0.017). The stomach contents (Table Sexual dimorphism 3) of females contained insects (92.2%), arachnids The mean SVL of sexually mature males (n = 73) (5.8%), crustaceans (0.6%), and plant material

Sexual dimorphism and natural history of the whiptail lizard 377

Table 1. Mean values (0.1 mm; 1 SE) and range of morphological characteristics (SVL = snout-vent length, IW = interaxial width, FL = forearm length, HW = head width, HH = head height, HL = head length, FEL = femur length, and TL = tibia length) of adult male and female Aspidoscelis costata from Isla Isabel, Nayarit, México (n = sample size). The statistical test is Mann-Whitney U-test.

Characteristics n Male n Female Z P SVL 73 67.9 (1SE: 1.1) (47.4-88.0) 35 67.6 (1SE: 0.79) (59.0-78.1) -0.266 > 0.05 HW 73 9.0 (1SE: 0.15) (6.0-12.9) 35 8.7 (1SE: 0.12) (7.4-10.4) -0.778 > 0.05 HH 73 8.2 (1SE: 0.18) (5.6-12.5) 35 7.6 (1SE: 0.14) (6.0-10.1) -1.723 > 0.05 HL 73 17.9 (1SE: 0.32) (10.0-23.9) 35 17.5 (1SE: 0.21) (15.2-20.4) -1.3 > 0.05 IW 73 32.6 (1SE: 0.53) (22.4-44.1) 35 33.7 (1SE: 0.52) (28-41.2) -1.382 > 0.05 FEL 73 10.1 (1SE: 0.18) (7.2-13.8) 35 9.9 (1SE: 0.14) (8.5-12.1) -0.394 > 0.05 FL 73 12.8 (1SE: 0.21) (8.4-16.6) 35 12.2 (1SE: 0.26) (10.0-17.5) -2.089 < 0.05 TL 73 15.3 (1SE: 0.25) (10.1-19.9) 35 14.6 (1SE: 0.18) (12.5-17.4) -2.022 < 0.05

Table 2. Reproductive characteristics of adult male and female Aspidoscelis costata from Isla Isabel, Nayarit, México. Mean is followed by 1 SE, and range is in parentheses; n = sample size.

Characteristics Male N Female N SVL (mm) 67.9 (1SE: 1.1) (47.4 – 88.0) 73 67.6 (1SE: 0.79) (59.0 – 78.1) 35 Liver mass (g) 0.20 (1SE: 0.01) (0.04 – 0.42) 73 0.22 (1SE: 0.01) (0.06 – 0.45) 35 Fat body mass (g) 0.05 (1SE: 0.01) (0.002 – 0.53) 73 0.07 (1SE: 0.01) (0.002 – 0.47) 35 Testes volume (mm3) 26.4 (1SE: 2.0) (0.908 – 82.01) 73 - - Vitellogenic follicles (mm3) - - 110.7 (1SE: 32.9) (2.5 – 443.4) 19 Oviductal eggs (mm3) - - 1,133.04 (1SE: 110.3) (716.8 – 1,350.9) 5 Vitellogenic follicles - - 2.9 (1SE: 0.23) (2 – 5) 19 Oviductal eggs - - 2.4 (1SE: 0.40) (2 – 4) 5

Table 3. Summary of the diet of Aspidoscelis costata from the Isla Isabel, Nayarit, Mexico. Males (n = 73) and females (n = 43; N = number of prey items; %N = percentage of items in total sample; S = number of stomachs containing items i; %S = percentage of stomach with item i; V = volume in mm3; %V = percentage of total volume; ViI = Impor- tance value of each prey category).

Female Male Prey category N %N S %S V %V ViI N %N S %S V %V ViI Arthropoda Arachnida Araneae 3 1.9 3 4.1 165.5 2.0 0.058 18 12.4 15 13.9 1,227.5 9.4 0.235 Acari 6 3.9 2 2.7 30 0.4 0.057 11 7.6 3 2.8 24.05 0.2 0.068 Crustacea 1 0.6 1 1.4 180 2.1 0.025 — — — — — — — Insecta Coleoptera 58 37.7 24 32.9 2,354 27.9 0.733 31 21.4 27 25.0 2,180.5 16.8 0.405 Dermaptera 1 0.6 1 1.4 0.5 < 0.01 0.018 — — — — — — — Hemiptera — — — — — — — 1 0.7 1 0.9 9 0.1 0.013 Hymenoptera 42 27.3 12 16.4 943.5 11.2 0.409 16 11.0 11 10.2 215 1.7 0.160 Isoptera 13 8.4 2 2.7 9.5 0.1 0.088 19 13.1 3 2.8 19 0.1 0.093 Orthoptera 28 18.2 26 35.6 4,726.5 56.0 0.904 45 31.0 44 40.7 9,129.5 70.2 0.924 Plant material 2 1.3 2 2.7 34 0.4 0.017 4 2.8 4 3.7 199.8 1.5 0.053 Totals 154 100 73 100 8,443.5 100 145 100 108 100 13,004.35 100

(1.3%), while prey items in male’s stomachs in- highest values of IV in males were for orthopter- cluded insects (77.2%), arachnids (20%), and plant ans (0.924) and coleopterans (0.405), while they material (2.8%). The mean prey volume for males were for orthopterans (0.904), coleopterans (0.733), (1625.5 mm3) and females (938.1 mm3) was statisti- and hymenopterans (0.409) in females. On the cally similar (t = -0.579, P = 0.574). Except for or- other hand, arachnids, dermapterans, hemipter- thopterans, the primary food source of both sexes, ans, isopterans, and plant material were of low the importance values for prey items consumed by importance for both sexes (Table 3). males and females were different (Table 3). The The diet breadth for A. costata revealed eight 378 R. Cruz-Elizalde et al. categories of prey consumed by males (B = 0.596), factors. Since clutch size is not associated with fe- and nine by females (B = 0.358). Diet overlap be- male SVL, they do not necessarily need to be lar- tween males and females was Ojk = 0.822, with a ger than males to maintain adequate reproductive percentage ranging from 66.2 to 100%. potential, as in A. marmorata and A. tesselata in the northern Chihuahuan Desert (Mata-Silva et al. 2010). Discussion However, mainland environments produce mostly different results with respect to sexual di- Sexual dimorphism morphism in body size, as males of several species Males larger than females are a typical pattern for tend to be significantly larger than females in sev- sexual dimorphism in lizards of the families Igua- eral populations (e.g., A. lineattissima, Ramírez- nidae, Tropiduridae, and Phrynosomatidae (Fitch Bautista et al. 2000; A. communis, Ramírez-Bautista 1978, Cox et al. 2007). However, only a few studies & Pardo-De la Rosa 2002; A. costata, Aguilar- have addressed sexual dimorphism in body size Moreno et al. 2010). The similarity in head size be- within the genus Aspidoscelis (e.g., Ramírez- tween males and females could be due to them Bautista et al. 2000, Ramírez-Bautista & Pardo-De eating similar-sized prey items in comparable la Rosa 2002, Aguilar-Moreno et al. 2010, Mata- quantities. It has been verified that arthropods on Silva et al. 2010), and for populations that occur on Isla Isabel are smaller, but more abundant than on islands (Dearing & Schall 1994). These authors the mainland (Andrews 1979). The main diet for point out that in species of Aspidoscelis males are both sexes on Isla Isabel consisted of small orthop- larger than females, indicating male-biased sexual terans and coleopterans, which might explain, in dimorphism. These outcomes could be based on part, why selection towards an enlarged head is phylogeny, which creates particular patterns, for apparently not present in this specific environ- example, the species of genus Uma, Callisaurus and ment. It is assumed that small and abundant Cophosaurus show sexual dimorphism male- grasshoppers and beetles in this island provide a biased, or within the spinosus species group of the sufficient source of energy for growth and repro- genus Sceloporus, males are larger than females duction, and consequently sustain the establish- (Fitch 1978). However, a recent study (Ramírez- ment of this population (Cooper & Vitt 1989). This Bautista et al. 2013) showed that males and fe- pattern supports the hypothesis that once indi- males of S. spinosus have similar SVL and other viduals from the mainland have established a morphological traits. Similarly, some species in the population on an island, they could attain a grammicus species group exhibited no size dimor- smaller size because the island environment favors phism (Hernández-Salinas et al. 2010). However, directional selection for smaller size (Foster 1964, these are generalizations based on scarce informa- Van Valen 1973), which probably is the case for tion from populations of each species. Conse- Isla Isabel, where abundant grasshoppers and bee- quently, evaluating potential drivers of sexual di- tles are smaller than their counterparts on the morphism in lizard species, including those with mainland. populations found in islands, such as A. costata, could provide useful insights. Reproductive characteristics The status of sexual dimorphism in A. costata The high testes volume in males and the high pro- populations from the mainland or from islands is duction of vitellogenic follicles and oviductal eggs poorly known (Hernández-Gallegos et al. 1998, in females during April 1977 and May 1981 sug- Aguilar-Moreno et al. 2010). In this study, males gests a synchronous reproductive activity between and females from Isla Isabel showed no sexual the sexes, a presumption discussed by Zaldívar- dimorphism in many morphological structures, Rae et al. (2008) for A. costata on Isla Isabel. In our including SVL (Table 1). The only exceptions were study, SVL at sexual maturity was smaller in in FL and TL. Sexual dimorphism in SVL and HL males (47.0 mm) than females (59.0 mm), although in species of non-territorial Aspidoscelis and Holco- mean SVL for both sexes was statistically similar. sus was attributed to sexual selection (Anderson & The population of A. costata from Isla Isabel also Vitt 1990), and niche divergence (Hierlihy et al. had a smaller SVL than populations from the 2013). However, morphological similarities in mainland (Aguilar-Moreno et al. 2010), and for some characters in males and females of A. costata other species from mainland areas as well from Isla Isabel could also be explained by other (Ramírez-Bautista et al. 2000, Ramírez-Bautista & Sexual dimorphism and natural history of the whiptail lizard 379

Pardo-De la Rosa 2002). The similarity in SVL be- 1993). Additionally, dietary shifts related to insect tween the sexes could be explained in terms of seasonal life cycles remain to be investigated. mean clutch size, which is low (2.4 eggs; Table 2), On the other hand, the insular population of with a frequency of at least three clutches during A. costata showed low values of food niche the reproductive season, as revealed by our find- breadth, and high overlap between sexes (0.822), ing of four females containing corpora lutea, eggs, like other mainland species of Aspidoscelis (Schall and vitellogenic follicles. This pattern was also 1993). These patterns are probably due to males found in another study on the same species on Isla and females from Isla Isabel selecting only two Isabel (Zaldívar-Rae et al. 2008). prey types (orthopterans and coleopterans) in- Most females encountered in April 1977 and stead of one (isopterans), as illustrated by many May 1981 had vitellogenic follicles and oviductal populations on the mainland (e.g., Schall 1993, eggs. Clutch size was not correlated with female Anderson 1993, Mata-Silva et al. 2013; Table 3). SVL, as reported by other studies on congeneric Prey preference by A. costata from Isla Isabel sug- species (Ramírez-Bautista et al. 2000, Ramírez- gests that these prey items likely provide sufficient Bautista & Pardo-De la Rosa 2002, Mata-Silva et al. energy for important metabolic activities, such as 2010). Clutch size was smaller than those found in growth, reproduction, and tissue repair of males species on the mainland, and can be explained in and females, as occurs in mainland species (e.g., A. two ways: first, females having a single clutch tigris and A. inornata, Pianka 1986, Schall 1993). during the reproductive period as a result of rela- Both males and females maintained a high tively low predation rates, and therefore a larger food volume during maximum reproductive activ- SVL is not needed to attain a larger clutch size or ity in April and May (Table 3). This pattern is longer offspring, as occurs with Aspidoscelis from similar to other congeneric species, indicating the the mainland (Ramírez-Bautista et al. 2002, Mata- necessity to maintain an active foraging mode in Silva et al. 2010); second, a small clutch size could order to obtain enough energy to survive until fe- be explained by high predation rates on lizards as males lay the eggs (Ramírez-Bautista & Pardo-De in many species of Aspidoscelis. As a result, females la Rosa 2002). However, due to the smaller clutch have evolved to have a higher clutch frequency size compared to those on the mainland, we as- (higher number of clutches during breeding sea- sumed that this energy is invested in offspring son); thus, females would invest more energy in SVL and not for clutch size (Ramírez-Bautista et al. reproduction than growth (Ramírez-Bautista & 2000). Vitt 1997). Finally, our results suggest important differences observed in reproductive and diet strategies Feeding characteristics performed by lizards living in islands from those The main types of prey consumed by males and living on the mainland. However, further studies females of A. costata are Orthoptera, Coleoptera, are necessary to fully understand the causes of dif- and Hymenoptera (Table 3). An insectivorous diet ferences in morphology, reproduction, and diet, as usually differs from that of many other island liz- well as other natural history attributes in this ard species, which have a herbivorous diet (Schall population. & Ressel 1991, Dearing & Schall 1992, Olensen & Valido 2003). The composition of the diet of A. costata from Isla Isabel differ from that of congeners on the mainland, whose primary prey items were Acknowledgements. We thank to Z. Uribe Peña for his termites (Isoptera; Milstead 1974, Anderson 1993, help in the field, and Arturo Rocha for reviewing the first Schall 1993, Menezes et al. 2011, Mata-Silva et al. version of the manuscript. We thank to D. Borges for his comments for improving the manuscript, also to two 2013), but it can also be similar to some species anonymous reviewers, who greatly improved our (e.g., Pack 1923, Medica 1967, Milstead & Tinkle manuscript. This study was supported in part by projects 1969, Taylor et al. 2011). It remains unknown if CONABIO JM001, and FOMIX CONACyT Hidalgo termites are less abundant on Isla Isabel than on 191908 "Diversidad biológica del Estado de Hidalgo the mainland. The diet of lizards from Isla Isabel (tercera etapa)". could also be the result of diurnal activities of both predator and prey (Dearing & Schall 1992, Olen- sen & Valido 2003), or prey preference due to maximum availability (Milstead 1974, Anderson 380 R. Cruz-Elizalde et al.

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