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Ecology of Xenosaurus rectocollaris in Tehuacan Valley, Puebla, Mexico.

Lizards of the genus Xenosaurus are viviparous dwellers of crevices and holes and they range throughout much of central and southern Mexico and into Guatemala (Ballinger et al., 2000b). All populations of Xenosaurus that have been examined are opportunistic foragers that consume a variety of prey, including arthropods and vertebrates, but primarily insects (e.g., Presch, 1981; Ballinger et al., 1995; Lemos-Espinal et al., 2003c, 2004; Garcia-Vazquez et al., 2009). However, there is some variation in ecological traits among species and populations, although it appears to be somewhat limited in extent. For example, reproductive characteristics, such as size of litter, the relationship between size of litter and size of female, size at maturity, and reproductive frequency appear to differ among and within populations and species of Xenosaurus (e.g., Smith et al., 2000; Lemos-Espinal and Rojas Gonzalez, 2000; Lemos-Espinal et al., 2003a, 2003b, 2004; Lemos-Espinal and Smith, 2005; Zamora-Abrego et al., 2007; Rojas-Gonzalez et al., 2008). Populations and species also vary in sexual dimorphism (Smith et al., 1997; Lemos-Espinal et al., 1996 1997, 2003a, 2004; Lemos-Espinal and Smith, 2005) and temperature relationships (Ballinger et al., 1995; Lemos-Espinal et al., 1996, 1997, 1998, 2003a, 2004; Lemos-Espinal and Smith, 2005). Thus, additional information on unstudied populations is needed to obtain a more complete understanding of the extent of variation in ecology and natural history among populations and species.

Given that some species and populations of Xenosaurus are classified as endangered or threatened by the Mexican government (e.g., Zuniga-Vega et al., 2007), and most species are known from relatively few and isolated populations (Ballinger et al., 2000b), it is critical that we gain a better understanding of their ecological needs and requirements so that appropriate management and conservation measures can be taken. To this end, we studied sexual dimorphism, reproduction, thermal ecology, and diet of a population of X. rectocollaris in Tehuacan Valley, Puebla, Mexico.

MATERIALS AND METHODS--The population we studied was in Tehuacan Valley, Puebla, Mexico (18[degrees]18'20.49"N, 97[degrees]28'55.44"W; 2, 100-2, 400 m elevation). Climate was subtropical with an average temperature and rainfall of 25.4[degrees]C and 401.2 mm, respectively (Garcia, 1988). Vegetation was a mixture of xerophilous plants: chaparral, palms (Brahea dulcis, B. nitida), yuccas (Yucca peliculosa, Y. oaxaquensis), agaves (Agave stricta, A. kerchovei, A. potatorum), green sotols (Dasylirion acrotiche), cactuses (Mytrocereus fulviceps, Echinocactus platyacanthus), and euforbs (cnidosculus tehuacanensis).

Lizards were collected by hand twice each month during 5 February 2003-14 July 2005. For each lizard, we measured snout-vent length with a plastic ruler (to nearest mm), mass with a spring scale (to nearest 0.1 g), body temperature (to nearest 0.1 [degrees]C) with a quick-reading cloacal thermometer (Miller and Weber, Inc., Ridgewood, New York) immediately upon capture. We also measured air temperature (shaded thermometer 1 cm above substrate where individual was first observed), and substrate temperature (shaded thermometer touching substrate where individual was first observed). We calculated thermal efficiency (E = 1-d[b.sub.mean]/d[o.sub.mean]) following Hertz et al. (1993). To evaluate the efficiency of thermoregulation, we used body temperature of 242 individuals taken in the wild, preferred body temperature of these individuals measured on a thermal gradient (16-45[degrees]C) in the laboratory, and operative temperature obtained by using hollow copper tubes that were sealed at each end, painted the same color as X. rectocollaris, and connected to a multimeter Extech model RH101 (Extech Instruments Corporation, Nashua, New Hampsire). Once a lizard was removed from its crevice, we placed the hollow copper model of appropriate size in its place and measured the temperature of the copper model (operative temperature) after allowing the temperature to equilibrate. Three lengths of copper tubing were used: 51, 67, and 98 mm, corresponding to lengths of neonates, juveniles, and adults, respectively (based on measurements on this and other studies of Xenosaurus; e.g., Zamora-Abrego et al., 2007). If the value of thermal efficiency is near zero, lizards do not thermoregulate efficiently (i.e., they are thermoconformers). Conversely, if thermal efficiency is near 1, lizards thermoregulate efficiently (i.e., they are thermoregulators).

A subset of the lizards (n = 60) were sacrificed and preserved shortly after collection (initially in 10% formalin, finally in 70% ethanol, and they were deposited in the herpetological collection of the Laboratorio de Ecologia of the Unidad de Biologia, Tecnologia y Prototipos). We measured width of head at the widest point, length of head from anterior edge of ear to tip of snout, and length of femur from knee to middle of pelvic region to the nearest 0.01 mm using calipers. Sexual dimorphism in width of head, length of head, and length of femur were analyzed using analysis of covariance with snout-vent length as the covariate after log transforming the dependent variables and the covariate (all three variables were significantly influenced by snout-vent length). unless noted, slopes in the ANCOVAs were homogeneous and interaction terms were removed from the final model. Means are given [+ or -] 1 SE.

We also dissected lizards to obtain information on size of litter and diet. Items in the diet were identified to order and percentage of volume for each taxon was calculated for each stomach (volume estimated by volumetric displacement to nearest [mm.sup.3]). We calculated the importance value of Powell et al. (1990).

RESULTS--Males were significantly smaller than females (snout-vent length of 73.3 [+ or -] 3.0 and 92.1 [+ or -] 2.4 mm for 24 males and 36 females, respectively; [F.sub.1,58] = 24.0, P < 0.01). Length of head did not differ significantly between males and females (15.3 [+ or -] 0.6 and 14.8 [+ or -] 0.5 mm for 24 males and 36 females, respectively; [F.sub.1,57] = 0.4, P = 0.55), but it was significantly related to snout-vent length ([F.sub.1,57] = 32.1, P < 0.01). Width of head did not differ between males and females (18.2 [+ or -] 0.4 and 17.9 [+ or -] 0.3 mm for 24 males and 36 females, respectively; [F.sub.1,57] = 0.3, P = 0.59), but it was significantly related to snout-vent length ([F.sub.1,57] = 120.6, P < 0.01). Length of femur of males and females did not differ (18.9 [+ or -] 0.5 and 18.8 [+ or -] 0.4 mm for 24 males and 36 females, respectively; [F.sub.1,57] = <0.1, P = 0.90), but it was related to snout-vent length ([F.sub.1,57] = 90.5, P < 0.01).

Mean total number of follicles was 9.6 [+ or -] 0.7 (range, 2-19, n = 30). Mean number of embryos was 2.6 [+ or -] 0.3 (range, 1-4, n = 11). Total number of follicles was neither related to snout-vent length (n = 30, [r.sup.2] = 0.01, P = 0.54) nor to total number of embryos (n = 11, [r.sup.2] = <0.01, P = 0.86). Mean mass of embryos was 2.6 [+ or -] 0.5 (n = 9) and it was not significantly related to snout-vent length of females (n = 9, [r.sup.2] = 0.13, P = 0.35).

Mean body temperature was 23.2 [+ or -] 0.3[degrees]C (range, 11.8-33.6, n = 242). There were significant differences in mean body temperature among categories of individuals within this population (Table 1; [F.sub.4,237] = 3.68, P = <0.01). Most notably, pregnant females maintained higher mean body temperature than non-pregnant females (Table 1).

Body temperature was related positively and significantly to air temperature (n = 242, [r.sup.2] = 0.51, P < 0.01, body temperature = 11.5 + 0.5 air temperature) and substrate temperature (n = 242, [r.sup.2] = 0.65, P < 0.01, body temperature = 8.6 + 0.6 substrate temperature) of the microhabitat occupied by the lizards. Little variation in body temperature was observed during the day (Fig. 1a). There was significant monthly variation in mean body, air, and substrate temperatures (Fig. 1b; body temperature: [F.sub.4,232] = 34.4, P < 0.01; air temperature: [F.sub.7,232] = 52.1, P < 0.01; [F.sub.4,232] = 68.2, P < 0.01).

Body temperature measured on a thermal gradient (16-45[degrees]C) in the laboratory and mean operative temperature were 30.4 [+ or -] 0.2[degrees]C (range, 26.0-33.4, n = 242) and 17.1 [+ or -] 0.3[degrees]C (range, 8-29, n = 568), respectively. Thermal efficiency of this population was 0.52 (Table 1).

Numerically, adult coleopterans were the most important food items and they dominated the diet (Table 2). Lepidopteran larvae were second in importance. Volumetrically, adult coleopterans and larval lepidopterans also were the two most important dietary items (Table 2). Adult coleopterans had the highest importance value, followed by larval lepidopterans (Table 2). Only one stomach contained vegetation, and no stomach contained vertebrate remains (Table 2). Eighteen lizards had empty stomachs.

[FIGURE 1 OMITTED]

DISCUSSION--In our study of X. rectocollaris, females were larger than males in snout-vent length. Not all species and populations of Xenosaurus are sexually dimorphic in size (e.g., X. grandis--Smith et al., 1997; Lemos-Espinal et al., 2003a), but in those where significant sexual dimorphism has been observed, females tend to be larger than males (e.g., X. newmanorum--Smith et al., 1997; X. phalareoantheron--Lemos-Espinal and Smith, 2005; X. platyceps--Lemos-Espinal et al., 1997, 2004). In another population of X. rectocollaris, males and females did not differ in snout-vent length (Lemos-Espinal et al., 1996).

There was no indication of sexual dimorphism in size of head or femur in the population of X. rectocollaris that we studied. In another population of X. rectocollaris, males and females also were not sexually dimorphic in these characters (Lemos-Espinal et al., 1996). This contrasts with most other studies of Xenosaurus, which have reported that males had larger heads and often larger femurs (e.g., X. grandis--Smith et al., 1997; Lemos-Espinal et al., 2003a; X. platyceps--Lemos-Espinal et al., 1997, 2004).

Mean estimated size of litter for the population we studied was 2.6. This is in the lower end of estimates for other Xenosaurus (e.g., Ballinger et al., 2000a; Lemos-Espinal and Rojas-Gonzalez, 2000; Lemos-Espinal et al., 2003 a, 2004; Zamora-Abrego et al. 2007; Zuniga-Vega et al., 2007; Rojas-Gonzalez et al., 2008), but is similar to the only other population of X. rectocollaris for which data were available (2.6; Zamora-Abrego et al., 2007). Estimated size of litter in the population we examined was not affected by size of female. The influence of snout-vent length of females on size of litter in Xenosaurus appears to be variable; some populations and species have a positive relationship (e.g., X. grandis--Ballinger et al., 2000a; X. platyceps--Ballinger et al., 2000a; Rojas-Gonzalez et al., 2008) and others exhibit no relationship (e.g., X. newmanorum--Ballinger et al., 2000 a; X. platyceps--Lemos-Espinal et al., 2004). Zamora-Abrego et al. (2007) detected a positive relationship between mean snout-vent length of females and mean size of litter for several species of Xenosaurus.

Mean body temperature of X. rectocollaris in Tehuacan Valley (23.2[degrees]C) is similar to that of a population of X. rectocollaris near Chapulco, Puebla (22.9[degrees]C; Lemos-Espinal et al., 1996). Both of these mean body temperature are within the range observed for Xenosaurus (X. grandis, 22.7[degrees]C--Ballinger etal., 1995; X. grandis agrenon, 25.6[degrees]C-- Lemos-Espinal et al., 2003a; X. newmanorum, 22.9[degrees]C--Lemos-Espinal et al., 1998; X. phalaroantheron, 20.3[degrees]C--Lemos-Espinal and Smith, 2005; X. platyceps,19.1-20.6[degrees]C--Lemos-Espinal et al., 1997, 2004). Our results suggest that the thermoregulatory strategy or ability of X. rectocollaris in the population we examined is intermediate between thermoregulating and thermoconforming, with suggestions that the strategy may be closer to the thermoconforming end of the spectrum (thermal efficiency = 0.52, indicating that body temperature is correlated strongly with environmental temperatures), which is consistent with observations of X. rectocollaris in Chapulco, Puebla (Lemos-Espinal et al., 1996). Several other populations of Xenosaurus appear to be thermoconformers (e.g., X. grandis--Ballinger et al., 1995; X. grandis agrenon--Lemos-Espinal et al., 2003a; X. newmanorum--Lemos-Espinal et al., 1998; X. phalaroantheron--Lemos-Espinal and Smith, 2005; X. platyceps--Lemos-Espinal et al., 1997, 2004). Indeed, body temperature of Xenosaurus appears to be limited by sun reaching the crevice (e.g., Lemos-Espinal et al., 1997).

Differences in body temperatures among different categories of individuals in the population were observed. In particular, pregnant females had higher body temperatures than non-pregnant females. Higher body temperatures in pregnant females than in non-pregnant females may suggest that pregnant females are seeking warmer microhabitats or locations within crevices. In other viviparous lizards, pregnant females often maintain their body temperature at different levels than non-pregnant females (e.g., Smith and Ballinger, 1994; Mathies and Andrews, 1997; Robert et al., 2006; Shine, 2006), possibly to improve the incubation environment and performance of their offspring (e.g., Wapstra, 2000; Rock and Cree, 2003; Shine, 2006; Ji et al., 2007). Frequently, these observations are associated with high-elevation lizards that experience cold climates; however, our results suggest that this pattern may also hold true for species whose typical habits preclude elevated body temperatures (e.g., a crevice-dwelling habit).

In general, species of Xenosaurus are believed to be opportunistic, or at least generalist, predators. Most studies of their diets have determined that they primarily consume insects (Ballinger et al., 1995; Lemos-Espinal et al., 2003c, 2004), but they also eat vertebrates, including mammals and lizards (Presch, 1981; Ballinger et al., 1995; Lemos-Espinal et al., 2003c; Garcia-Vazquez et al., 2009), and some vegetation (Lemos-Espinal et al., 2003c). Our analyses of diet are consistent with previous studies, but suggest that the population we studied may consume beetles more than some other populations. It is unclear whether abundance of beetles reflects local availability or a local preference.

In conclusion, the ecology and natural history of the population of X. rectocollaris that we studied is within the range of previously observed variation in species and populations of Xenosaurus. When combined with previous studies, our results suggest that the natural history and ecology of Xenosaurus is fairly constant; perhaps, as a function of constraints imposed by the crevice-dwelling habit that all species of this genus share. In addition to conserving appropriate macrohabitats, our study suggests that requirements for successful conservation of these lizards will likely be similar among species (e.g., conserving appropriate crevices or holes for them to live in).

This study was supported by projects Consejo Nacional de Ciencia y Tecnologia 40797-Q, Programa de Apoyo a Proyectos de Investigation e Innovation Tecnologica IN 208398, IN 216199, IN 200102, and Proyecto Anual para Profesores de Carrera 2003 Procesos espaciales en la diversidad local y regional de los ensambles de reptiles del Valle de Tehuacan-Cuicatlan y el norte del desierto Chihuahuense and Proyecto Anual para Profesores de Carrera 2007 Organization ecologica del ensamble de lagartijas en el Valle de Zapotitlan Salinas, Puebla. We thank D. Leavitt and an anonymous reviewer for comments that improved the manuscript.

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Submitted 28 June 2010.

Accepted 23 January 2012.

Associate Editor was Geoffrey c. carpenter.

GUILLERMO A. WOOLRICH-PINA, JULIO A. LEMOS-ESPINAL, LUIS OLIVER-LOPEZ, AND GEOFFREY R. SMITH *

Laboratorio de Ecologia, Unidad de Biologia, Tecnologia y Prototipos (Facultad de Estudios Superiores-Iztacala,

Universidad Nacional Autonoma de Mexico), Avenida de los Barrios S/N, Los Reyes Iztacala,

Tlalnepantla, Estado de Mexico, 54090 Mexico (GAW-P, JAL-E, LO-L)

Department of Biology, Denison University, Granville, OH 43023 (GRS)

* Correspondent: smithg@denison.edu
TABLE 1--Body temperature (mean [+ or -] 1 SEE) and thermal
efficiency of various categories of Xenosaurus rectocollaris in
Tehuacan Valley, Puebla, Mexico. Means sharing the same letter
are not significantly different (Tukey HSD, P < 0.05).

                                  Temperature        Thermal
Category                 n       ([degrees]C)       efficiency

Males                   55    23.0 [+ or -] 0.6AB      0.54
Pregnant females        45    24.4 [+ or -] 0.5A       0.57
Non-pregnant females    62    22.0 [+ or -] 0.5B       0.48
Juveniles               38    24.5 [+ or -] 0.6A       0.62
Neonates                42    22.3 [+ or -] 0.5B       0.42
overall                242    23.2 [+ or -] 0.3        0.52

TABLE 2--Diet of Xenosaurus rectocollaris in Tehuacan Valley,
Puebla, Mexico. Importance value follows Powell et al. (1990) and
is the sum of the percentages of number of stomachs containing a
prey taxon, number of a prey taxon consumed, and total volume of a
prey taxon consumed.

Taxon                  Number of     Number of    Total Volume
                      stomachs (%)   items (%)   ([mm.sup.3] %)

Arachnidae              5 (7.7)       5 (7.5)      2.55 (9.0)
Adult Coleoptera       30 (46.1)     34 (50.8)    12.65 (44.5)
Larval Coleoptera       4 (6.2)       5 (7.5)      2.39 (8.4)
Larval Diptera          4 (6.2)       4 (6.0)      1.30 (4.6)
Hymenoptera (ant)       1 (1.5)       1 (1.5)      0.04 (0.1)
Adult Lepidoptera       1 (1.5)       1 (1.5)      0.18 (0.6)
Larval Lepidoptera     10 (15.3)     11 (16.4)    4.61 (16.2)
Millipede               1 (1.5)       1 (1.5)      0.50 (1.8)
Adult orthoptera        2 (3.1)       2 (3.0)      1.16 (4.1)
Larval Orthoptera       3 (4.6)       3 (4.5)      1.18 (4.1)
Vegetation              1 (1.5)          -         0.35 (1.2)
Unidentified            2 (3.1)          -         1.54 (5.4)
Empty                  18 (27.7)         -             -
Total                      65           67           28.44

Taxon                 Mean volume   importance
                       per item       value

Arachnidae               0.51          24.2
Adult Coleoptera         0.38         141.4
Larval Coleoptera        0.48          22.1
Larval Diptera           0.33          16.8
Hymenoptera (ant)        0.04          3.1
Adult Lepidoptera        0.18          3.6
Larval Lepidoptera       0.42          47.9
Millipede                0.50          4.8
Adult orthoptera         0.58          10.2
Larval Orthoptera        0.39          13.2
Vegetation                 -            -
Unidentified               -            -
Empty                      -            -
Total
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Author:Woolrich-Pina, Guillermo A.; Lemos-Espinal, Julio A.; Oliver-Lopez, Luis; Smith, Geoffrey R.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Jun 1, 2012
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