INTRODUCTION

The genus Sceloporus Wiegmann, 1828 is composed of 97 species (Leaché et al., 2016). These species have shown high variation in ecological, morphological, and reproductive attributes (Benabib, 1994; Leyte-Manrique and Ramírez-Bautista, 2010; Zúñiga-Vega et al., 2016; García-Rosales et al., 2017) both at the intraspecific (Stephenson, 2010; García-Rosales et al., 2017) and the intrapopulation level (Ramírez-Bautista et al., 2008, 2014, 2016a, b).

With respect to lizard species (Cox et al., 2003, 2007), in the genus Sceloporus (Fitch, 1978; Jiménez-Arcos et al., 2017) morphological variation between sexes, also called sexual dimorphism, has been explained by two main hypotheses: (i) male-biased dimorphism by sexual selection, which gives advantages in male-male competition for territory and access to females (Endler and Houde, 1995) and (ii) female-biased dimorphism explained by fecundity advantage, where larger females are favored by natural selection (Du et al., 2005; Pincheira-Donoso and Hunt, 2017). A third hypothesis proposed by Rand (1967) and Schoener (1967) suggests that sexual dimorphism in lizards has evolved by intraspecific niche divergence, in which each sex is able to use the same or different resources with different degrees, such as food, microhabitat, and territory (Schoener, 1967; Hierlihy et al., 2013); however, this hypothesis has only been tested in a few studies (Herrel et al., 2001; Edwards et al., 2013).

According to Fitch (1978), the genus Sceloporus shows three patterns of sexual dimorphism that have been confirmed in recent years by several studies: (i) larger snout–vent length (SVL) in males than in females found in S. torquatus Wiegmann, 1828, S. grammicus Wiegmann, 1828, and S. minor Cope, 1885 (Feria-Ortíz et al., 2001; Hernández-Salinas et al., 2010; Ramírez-Bautista et al., 2014); (ii) larger female SVL than male SVL found in S. undulatus (Bosc and Daudin in Sonnini and Latrelle, 1801), S. graciosus Baird and Girard, 1852, and S. virgatus Smith, 1938 (Fitch, 1978; Cox and John-Alder, 2007); and (iii) lack of sexual dimorphism found in S. taeniocnemis Cope, 1885, S. formosus Wiegman, 1834, and S. spinosus Wiegmann, 1828 (Fitch, 1978; Ramírez-Bautista and Pavón, 2009; Ramírez-Bautista et al., 2013). Likewise, at the population level several studies have reported temporal (Ramírez-Bautista et al., 2016a) and geographic variation in sexual dimorphism (Valdéz-González and Ramírez-Bautista, 2002; Ramírez-Bautista et al., 2013). These patterns have been explained by the effect of sexual competition (Fitch, 1978; Ramírez-Bautista et al., 2008; Ramírez-Bautista and Pavón, 2009), different degrees of growth rate between sexes (Ruby and Dunham, 1984; Smith and Ballinger, 1994), fecundity (Olsson et al., 2002; Pincheira-Donoso and Hunt, 2017), and niche divergence (Camilleri and Shine, 1990; Hierlihy et al., 2013).

Morphological variation and sexual dimorphism can affect the ecology and behavior of individuals, mainly in the use of food resources (Edwards et al., 2013; Scali et al., 2016). This parameter is indispensable for maintenance and development, such as growth, reproduction, and tissue repair in lizard species (Vitt and Caldwell, 2009); therefore, the quantity and quality of consumed food are important parameters influencing these activities (Ballinger and Congdon, 1980). Use of food resources by both sexes and among populations are determined by food availability in the environment. Such availability might be influenced by the dry and wet seasons as well as intrainterspecific competition (Huey and Pianka, 1981; Ngo et al., 2015). For example, variation has been recorded in the diet composition between insular and mainland populations (Dutra et al., 2011; Hernández-Salinas et al., 2016) or among populations from different mainland environments (Parker and Pianka, 1975; Ngo et al., 2015). Likewise, diet type can vary in relation to type, size, and abundance of prey consumed between sexes and populations (Vitt and Colli, 1994; Herrel et al., 2001).

Sceloporus aeneus Wiegmann, 1828 is an endemic species of Mexico, oviparous, and of small size in SVL (47–50 mm). Its distribution occurs in the central and northern regions of the country, in the states of Puebla, Michoacán, Guanajuato, Morelos, Estado de México, Distrito Federal, and Hidalgo (Smith et al., 1993). It inhabits temperate environments from high elevation with vegetation types of pine, oak, and pine-oak forests (Sites et al., 1992). Studies carried out among populations of this species have shown similarities in reproductive characteristics, such as clutch size, egg mass, and volume (Rodríguez-Romero et al., 2002; Manríquez-Morán et al., 2013; Ramírez-Bautista et al., 2016b) as well as differences in minimum SVL at sexual maturity (Manríquez-Morán et al., 2013; Ramírez-Bautista et al., 2016a, b). Regarding sexual dimorphism, it has been reported that males show larger SVL than females (Ramírez-Bautista et al., 2016a). Despite showing similarities in reproductive characteristics and morphological variation among populations, there is no information to date on the use of food resources between sexes and/or seasons within a population. Such ecological studies are needed to determine possible interactions that could help interpret the variations/similarities of the reproductive and morphological attributes, which will also generate information on the feeding behavior of the species, and between sexes and seasons within the same population.

Therefore, the goal of this study was to analyze sexual dimorphism as well as feeding ecology between sexes and seasons of Sceloporus aeneus from central Mexico. The objectives comprised: (i) to analyze sexual dimorphism, (ii) to determine the diet in both females and males within seasons, (iii) to determine the degree of overlap of the food niche between sexes and seasons, and (iv) to determine the relationship between sizes (SVL) of the individuals and the volume and weight of stomach contents, as well as abundance of consumed prey. According to the hypothesis on variation of morphological characteristics previously found between sexes (Ramírez-Bautista et al., 2016a), we expected to find differences in the diet between sexes and seasons, as well as a low overlap in the use of food resources.

MATERIALS AND METHODS

RESULTS

Diet

A total of 62 (42 females and 20 males) lizards were collected for the analyses of stomach contents. These lizards fed on a total of 783 prey items belonging to 11 categories (Table 2). The diet of Sceloporus aeneus (Table 2) was composed primarily of insects (70%), followed by arachnids (20%), and plant material (10%).

For the population estimate, the prey categories Formicidae, Coleoptera (adult; A), and Hemiptera showed the highest values of food importance (I), as well as being the most consumed prey in the population (Table 2). When diet was analyzed by sex, females consumed 11 prey categories, and males 9; however, no significant difference was found (U = 42.5, P = 0.250). According to the abundance of prey consumed, no significant difference was found (U = 42.5, P = 0.621) between males (38.22 ± 28.05) and females (39.90 ± 21.28; Table 2). The categories Formicidae, Coleoptera (A), and Hemiptera in females, and Orthoptera in males showed the highest values of I. For females, these values were 28.63, 23.62, and 22.62 for Formicidae, Coleoptera (A), and Hemiptera, respectively. In males, the values for Formicidae, Coleoptera (A), and Orthoptera were 44.64, 26.61, and 8.65, respectively (Table 2).

Table 1.

Mean values ± 1 SE and range of morphological characteristics (SVL = snout–vent length, JW = jaw width, JL = jaw length, FEL = femur length, TL = tibia length, FL = forearm length) of adult female and male Sceloporus aeneus from El Encinal, Cuautepec de Hinojosa, Hidalgo, Mexico. Comparisons were made with ANCOVA with SVL as the covariate.

Table 2.

Diet composition of the species, females, and males of Sceloporus aeneus from El Encinal, Cuautepec de Hinojosa, Hidalgo, Mexico. N = number of items, F = frequency of occurrence, and I = value of feeding importance. A = adult, L = larvae.

Diet composition by season

Diet composition showed similarity between seasons (U = 42, P = 0.838). In the dry season, a lower number of prey categories (eight) but more prey items (439) were found compared to the wet season (10 prey categories and 340 prey items; Table 3). The number of prey items consumed in the dry (54.87 ± 34.99) and the wet (34 ± 20.04) season did not differ significantly (U = 32, P = 0.505). For the dry season, the categories Formicidae, Hemiptera, Coleoptera (A), and Orthoptera showed the highest values of I (Table 3). For the wet season, the results revealed a very similar composition of prey categories to those of the dry season (Formicidae, Coleoptera [A], and Orthoptera); however, the category Coleoptera (larva; L) also recorded high values of I (Table 3).

Table 3.

Diet composition of Sceloporus aeneus from El Encinal per season (Dry [January–June and October–December] and Wet [July–September]). n = number of items, I = Value of feeding importance. A = adult, L = larvae.

DISCUSSION

Sceloporus aeneus, like other species of the genus, shows male-biased sexual dimorphism (Fitch, 1978; Ramírez-Bautista et al., 2016a; Jiménez-Arcos et al., 2017). This pattern is similar to that of other small-sized species, such as S. gadoviae Boulenger, 1905 (Lemos-Espinal et al., 1999), S. siniferus Cope, 1870 (Hierlihy et al., 2013; Ramírez-Bautista et al., 2015), and S. variabilis Wiegmann, 1834 (Ramírez-Bautista et al., 2006; Cruz-Elizalde et al., 2017).

Males of Sceloporus aeneus showed sexual dimorphism in dimensions of the jaws and limbs, but not in SVL or JL (see Table 1). This pattern of sexual dimorphism is similar to that found in other populations of the same species from central Mexico (Ramírez-Bautista et al., 2016a). As in other species of the genus, in addition to the morphological characteristics, sexual dimorphism can be expressed in other attributes such as color pattern (Stephenson and Ramírez-Bautista, 2012; Jiménez-Arcos et al., 2017). Males of S. aeneus show more conspicuous ventral and gular patches than females (Smith et al., 1993). This color pattern has been evaluated for species that lack sexual dimorphism in body size like S. torquatus (Feria-Ortíz et al., 2001), S. formosus (Ramírez-Bautista and Pavón, 2009), and S. spinosus (Ramírez-Bautista et al., 2013). These color patterns are used by males for intra-interspecific recognition, care, and defense of territory and courtship (Martins, 1994; Cox et al., 2003; García-Rosales et al., 2017).

Figure 1.

Relationships between snout–vent length (SVL) and volume of stomach contents of females (A) and males (B), and SVL vs. mass of stomach content in females (C) and males (D).

Despite not showing significant differences in SVL and JL between sexes, the rest of the analyzed characteristics varied, with the males having the greatest morphological dimensions. These results can be explained by the sexual selection hypothesis (Cox et al., 2003, 2007), because the greatest dimensions in the jaw (or the head) give an advantage in the male-male combat to gain access to the females and in the defense of the territory (Fitch, 1978; Cox et al., 2003). This pattern occurs in other species of the genus such as Sceloporus minor (Ramírez-Bautista et al., 2014) and S. grammicus (Hernández-Salinas et al., 2010; Bastiaans et al., 2014), as well as in other lizard species like Zootaca vivipara (Lichtenstein, 1823) (Gvozdik and Van Damme, 2003) and Lacerta agilis Linnaeus, 1758 (Borczyk et al., 2014). In this sense, intersexual competition (Fitch, 1978; Ramírez-Bautista et al., 2008; Ramírez-Bautista and Pavón, 2009), unlike fecundity (Olsson et al., 2002) and different growth rates in each sex (Ruby and Dunham, 1984; Cox and John-Adler, 2007), may be determining the morphological differences between the sexes of this species (Ramírez-Bautista et al., 2016a).

Morphological variation can be influenced by diverse factors, such as sexual selection (Fitch, 1978; Cox et al., 2003), competition (Parker and Pianka, 1975; Olsson et al., 2002), or use of resources (Scali et al., 2016). Therefore, this morphological variation is highly related to the ecology and reproductive characteristics of the individuals, which is also reflected in the use of food resources (Miles et al., 2007). The analyzed population of Sceloporus aeneus showed an insectivore diet, similar to other species of the genus, like S. grammicus (Leyte-Manrique and Ramírez-Bautista, 2010) and S. jarrovii Cope in Yarrow, 1875 (Gadsden et al., 2011), as well as other lizard species such as Eutropis multifasciata (Kuhl, 1820) (Ngo et al., 2014), Anolis nebulosus (Wiegmann, 1834) (Hernández-Salinas et al., 2016), Xenosaurus mendozai Nieto-Montes de Oca et al., 2013 (Zamora-Abrego and Ortega-León, 2016), and Tropidurus torquatus (Wied, 1821) (Siqueira et al., 2013).

The main prey categories consumed by Sceloporus aeneus were from the Formicidae family and the orders Hemiptera and Coleoptera (A), which coincides with the diet patterns of other species of the genus like S. grammicus (Leyte-Manrique and Ramírez-Bautista, 2010) and S. jarrovii (Gadsden et al., 2011). These results are also similar to those reported for other species from temperate environments of central Mexico, such as S. mucronatus Cope, 1885 (Méndez-de La Cruz et al., 1992) and S. torquatus (Feria-Ortíz et al., 2010). Diet composition may be influenced by the foraging mode of the species, which are classified as “sit and wait” (Huey and Pianka, 1981; Reilly et al., 2007), a characteristic of the genus Sceloporus. In addition, diet might also be determined by the availability of the resources in the environment (Ballinger and Ballinger, 1979) because variation in precipitation or temperature modifies the biomass of the food that lizards can consume (Ballinger, 1977; Benabib, 1994).

Diet composition similar to that indicated above has been observed in other lizard species of the same genus, such as Sceloporus gadoviae, S. horridus Wiegmann, 1834, S. jalapae Günther, 1890 (Serrano-Cardozo et al., 2008), S. grammicus (Leyte-Manrique and Ramírez-Bautista, 2010), and S. jarrovii (Gadsden et al., 2011), and in species of a different genus, such as Xenosaurus mendozai (Zamora-Abrego and Ortega-León, 2016). In these species, seasonal changes in diet have been reported in relation to prey availability of Hymenoptera, Formicidae, Coleoptera, or Hemiptera, whose abundances are influenced by rains or droughts throughout the year. The latter results in a diet composition that is significantly shaped by the occurrence and abundance of the available categories in the environment (Ballinger and Ballinger, 1979). This pattern of seasonal change might also occur in this population of S. aeneus, because even though they consumed a smaller number of prey categories (8) in the dry season than in the wet season (10), total abundance of prey was greater in the dry period than during the rains, and no significant difference was found. Ballinger and Ballinger (1979) pointed out that the differences in the number of consumed prey by season might be affected by the low availability of prey in the environment, especially of prey that are gregarious such as ants, hemipterans, and coleopterans. Therefore, individuals in the population would consume a high number of prey of small size, such as ants, to compensate for the nutritional value that larger prey can provide, such as members of Coleoptera or Lepidoptera (Maury, 1995; Gadsden et al., 2011).

Similarly, an increase in the volume of stomach contents, as well as the consumption of a higher number of prey categories, might be related to the different phases of the reproductive period, and, thus, to the different types of diet between sexes. For example, in viviparous species such as Sceloporus mucronatus (Méndez-de La Cruz et al., 1992), S. torquatus (Feria-Ortíz et al., 2001), and S. jarrovii (Gadsden and Estrada-Rodríguez, 2008) the lowest volume of stomach content in females coincides with the gestation period; therefore, the embryos would displace the stomach of the lizards and occupy more space inside the females. When neonates are born, the production of progesterone in the females decreases (Crews and Garrick, 1980) and feeding increases, as does the volume of stomach contents (Méndez-de La Cruz et al., 1992). With regard to S. aeneus, it has been reported that different populations in central Mexico produce at least two clutches (frequencies) during the reproductive season (Rodríguez-Romero et al., 2002; Manríquez-Morán et al., 2013; Ramírez-Bautista et al., 2016b). This reproductive pattern allows females to consume a constant volume of food, and this consumption rate can be increased and converted to energy invested in reproduction, as has been observed in oviparous species like S. variabilis (Benabib, 1994). These results might explain the higher value reported for breadth of food niche in females than in males at the population and season level, and the higher volume of stomach contents in the dry season and previous to the months of the reproductive activity of the females (April–September; Ramírez-Bautista et al., 2016b); also, no correlation was observed between female SVL and volume of stomach contents. The above indicates that the females might feeding continuously throughout the year (Benabib, 1994) and investing energy on egg production (clutch size, egg mass and volume) without significant changes among reproductive periods or populations (Manríquez-Morán et al., 2013; Ramírez-Bautista et al., 2016a, b).

In males, the diet was composed of a smaller number of categories, but with greater abundance of prey consumed than in females, until no significant difference was found. Similar pattern has been reported for other species, such as Anolis nebulosus (Lister and Aguayo, 1992), A. humilis Peters, 1863 (Parmerlee and Guyer, 1995), and A. polylepis Peters, 1874 (Perry, 1996). This result may be due to the fact that reproduction in males of Sceloporus aeneus represents a higher energy cost, mainly for defense of territory and access to females (Martori and Aun, 1997). This energy cost is compensated by feeding on a smaller number of prey but containing a higher nutritional value, such as members of Orthoptera or Coleoptera (Maury, 1995). In addition, the foraging time invested by males can be different from that of females, which modifies the number of prey consumed, as well as the values of breadth of food niche between seasons (Perry, 1996; Hierlihy et al., 2013).

Sceloporus aeneus, like other species of the S. scalaris group (Benabib et al., 1997; Rodríguez-Romero et al., 2002; Leaché et al., 2016), maintains similar characteristics among its populations, such as body size (SVL; Rodríguez-Romero et al., 2002; Ramírez-Bautista et al., 2016a), reproductive characteristics (Manríquez-Morán et al., 2013; Ramírez-Bautista et al., 2016a, b), and ecological characteristics (Smith et al., 1993; Benabib et al., 1997; Rodríguez-Romero, 1999). The absence of sexual dimorphism with respect to body size (SVL) recorded in this study was different to the general pattern reported in the genus Sceloporus, where males are larger than females in SVL (Fitch, 1978; Jiménez-Arcos et al., 2017). However, in this study the rest of the morphological structures (mandibular and body extremities) coincide with male-biased dimorphism in the genus (Fitch, 1978; Wiens, 1999). Morphological differences can influence other activities, such as the use of available resources both at the intrapopulation and interpopulation level; therefore, alongside analyzing the use of food resources between sexes and seasons, further studies are needed aiming to evaluate different populations of single species, as well as the effect of food on reproductive characteristics (e.g., clutch size, egg mass and volume; Hernández-Salinas et al., 2016), growth rate (Ballinger and Congdon, 1980; Duncan et al., 2015), and cranial morphology (Herrel et al., 2008; Edwards et al., 2013).