Herpetology Notes, volume 10: 161-167 (2017) (published online on 19 April 2017)
Natural History of Sceloporus goldmani (Squamata: Phrynosomatidae) in its southern distribution
Rubén Alonso Carbajal-Márquez1, 3,* and Gustavo Ernesto Quintero-Díaz2, 3
Introduction. frequency of appearance (FA) was calculated as the total frequency of a component, divided by the total number The bunchgrass lizard Sceloporus goldmani Smith, of scats. To consider the importance of all species, the 1937, belonging to the S. scalaris group, was believed percentage of occurrence (PA) was also calculated as the to be extinct due to habitat destruction, and surveys total frequency of a component, divided by the sum of with unsuccessful results in the historical localities in all frequencies (Aranda et al., 1995). The activities were the states of Coahuila, Nuevo León and San Luis Potosí, carried out under authorization of scientific collection for this reason have not been included in the most recent through document number SGPA / DGVS / 05143/14 analyses (Smith and Hall, 1974; Thomas and Dixon, and SGPA / DGVS / 030709/16. 1976; Sinervo et al., 2010; Bryson et al., 2012; Leaché et al., 2013; Grummer et al., 2014; Grummer and Bryson, Results. 2014). Recently new populations of this species were found in the states of Aguascalientes, Jalisco, San Luis Morphology. The specimens of Sceloporus goldmani Potosí and Zacatecas (Carbajal-Márquez and Quintero- reported here agree with the characters of Smith’s (1937) Díaz, 2016). Here we provide a brief description of original description. The specimens (N = 21; 10 males, these new specimens, as well as observations on their 11 females) measured on average 44.08 mm ± 11.15 mm natural history, which until now were poorly known. snout vent length (SVL), and the largest specimen was a female with 57.7 mm SVL; average total length (TL) Materials and methods. 83.27 mm ± 31.27 mm , and the largest TL was 111 mm in both sexes. They weighed on average 3.14 g ± 1.16 g; The counting of scales and morphological characters males weighed on average 3.41 g ± 0.69 g, and females were carried out based on the work of Smith (1937). The weighed 2.88 g ± 1.44 g. The average number of dorsal measurements were performed with a digital vernier scales was 52.62 ± 1.60, the average for ventral scales micrometric calibrator (resolution of ± 0.1 mm). The was 39.38 ± 4.42. They have 30-38 femoral pores in weight was obtained with a digital balance (resolution of series, separated by no more than two scales ± 0.1g). To determine diet, the scats were obtained from the specimens by palpation of the abdominal region Coloration. The coloration in life is as follows: the and analysed under a stereoscopic microscope. The background colour is grey or light brown; the top of the head generally has three to five dark brown spots, occasionally another five spots are present in the neck; in the dorsal region of the trunk there are thirteen to 1 El Colegio de la Frontera Sur. Departamento de Conservación fifteen pairs of dark brown or black crescent-shaped de la Biodiversidad. Unidad Chetumal. Av. Centenario Km marks bordered by white scales, and located between 5.5, 77014, Chetumal, Quintana Roo, México. a pair of clear lines that are cream or light yellow, 2 Universidad Autónoma de Aguascalientes, Centro de Ciencias ranging from the neck to the base of the tail. Below Básicas, Departamento de Biología, Avenida Universidad these lines, presents another series of equal number of No. 940, Aguascalientes, Ags. 20131, México. dark marks but smaller than those on the back. The tail E-mail: [email protected] has a series of six to twelve dark marks on the dorsum, 3 Conservación de la Biodiversidad del Centro de México, A. C. Andador Torre de Marfil No. 100, C. P. 20229, sometimes fused (Fig. 1, 2). The throat of the males is Aguascalientes, Aguascalientes, México. slightly barred with black marks, and in females this * Corresponding author e-mail: [email protected] barring is less perceptible; in the belly the males have 162 Rubén Alonso Carbajal-Márquez & Gustavo Ernesto Quintero-Díaz
Figure 1. Male specimen of Sceloporus goldmani.
Figure 2. Female specimen of Sceloporus goldmani.
two pale blue abdominal marks (semeions) separated belly with some scattered black dots and they present by six to eight scales, and interrupted by black spots, reddish tones in the armpit when they are pregnant (Fig. and in reproductive season they present in the armpit an 4). Both sexes have a black spot on the shoulders, and orange dorsolateral patch that extends approximately to on the spot they have one to three blue scales that in the middle of the body (Fig. 3), the females have a white most cases are in the anterior region of that spot. In Natural History of Sceloporus goldmani in its southern distribution 163
Figure 3. Ventral view of a male specimen of Sceloporus goldmani.
none of the specimens of the new populations was the Activity and behavior. They are diurnal lizards, having patternless phase observed. their activity in the morning and afternoon, and reducing Diet. Twenty one (21) scats belonging to 19 specimens their activity during the warmer hours of the day. They collected between February to June were analysed. Three prefer open sites where the vegetation is not very high, orders belonging to Hexapoda were found, the most and are usually found near shrubs, cactus (Opuntia) or important orders being Homoptera and Hymenoptera, rocks. A greater number of lizards were observed on as well as plant remains; (Table 1). the edges of the plateaus with slight inclination, areas with abundant rocks and scarce vegetation, and some Reproduction. On May 29, 2013 at 10:40 am, the mating behaviour was observed in the field, the male bit specimens were observed around anthills produced by the female’s tail and the female turned to bite the nape of the male forming a ring with their bodies, exposing the white belly that contrasted with the grass beneath, making them perhaps vulnerable to being depredated. Table 1. Diet pertaining to 21 scats of 19 specimens found 1 TABLE 1. Diet pertaining to 21 scats of 19 specimens found during this study (N = number of samples in which As we approached, they remained in that position for during this study (N = number of samples in which it at least five minutes, until the male 2released it appears, the female FA = Frequency appears, of appearance, FA = Frequency PA = Percentage of appearance, of appearance). PA = Percentage of and both tried to escape (Carbajal-Márquez et al., 2013). appearance). Neonates were observed on May 11,3 2014, as well as a pregnant female and a hatchling on June 13, 2013. ORDER N FA PA In order to verify if they were viviparous lizards, two Coleoptera 5 23.8 9.8 females were collected in February 2014, both gave Homoptera 21 100 41.1 birth to seven and eight offspring respectively on June Hymenoptera 19 90.4 37.2 11, 2014. The offspring are miniature replicas of adults Plant Remains 6 28.5 11.7 (Fig. 5). 4
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26 164 Rubén Alonso Carbajal-Márquez & Gustavo Ernesto Quintero-Díaz
Figure 4. Ventral view of female specimen of Sceloporus goldmani.
Pogonomyrmex sp. When the lizards are discovered The coloration of S. goldmani is very similar to they undertake a race to hide under some creeping shrub other species in the S. scalaris group, highlighting the or cactus, or inside a burrow usually located under a presence of dark bars in the throat in both sexes, but rock, if there are no nearby shelters, they hide under the more evident in males. In addition the presence of pale grass, adopting a U- shaped position, or they try to go blue abdominal marks (semeions) interrupted by black unnoticed on the surface of the large, flat rocks, which spots in the males, and in females only the presence of they use as perfect camouflage. Some individuals were abdominal tenuous black spots (Smith, 1939). Another observed foraging, and at the moment of our approaching point of similarity with other species in the S. scalaris they undulated the tail parallel to the ground, perhaps as group is that males have an orange patch on the axilla an antipredator behaviour. Most of the specimens were that extends mid-body in breeding season. Additionally found with an approximate separation of 10 to 15 meters it is important to note the absence of a patternless between each of them. ������������������������������� phase. was observed from middle February to November, with There are few published studies that address the more activity in the early rainy season. diet of species belonging to the S. scalaris group. The diet reported for S. brownorum in Aguascalientes Discussion. comprised the Hexapoda orders: Coleoptera, Diptera, Hymenoptera and Orthoptera; and Arachnida: Araneae Comparison with other members of the Scalaris (Vázquez-Díaz and Quintero-Díaz, 2005). Sceloporus group bicanthalis in the Tehuacán-Cuicatlán Valley feeds on The main differences of S. goldmani with the rest of the Hexapoda: Homoptera, Hemiptera, Coleoptera, the species of the S. scalaris group are the presence of Hymenoptera, and Arachnida: Araneae (Canseco- the lateral scales in definitely oblique rows, not parallel Márquez and Gutiérrez-Mayen, 2010). The diet of S. with respect to the dorsal; the number of dorsal scales slevini in Chihuahua consists of Hexapoda: Coleoptera, greater than 50; a short tail, and the viviparity . Due to Hemiptera, Hymenoptera and Orthoptera (Lemos- the obtained measurements of SVL and TL, S. goldmani Espinal and Smith, 2009). In all these cases the diet can be considered a small sized species of the S. scalaris was more diverse at the order level, than that found group (Watkins-Colwell et al., 1998). in S. goldmani, perhaps due to the seasons in which Natural History of Sceloporus goldmani in its southern distribution 165
Figure 5. Female of Sceloporus goldmani in labor and four neonates.
our samplings were carried out, or our sample size; which justifies the confusion in the identification of the although the previous authors do not report the date and specimens, since the presence of S. goldmani was not sample size. expected in Aguascalientes. Only S. bicanthalis shares viviparity with S. goldmani Members of the S. scalaris group are strictly terrestrial in the S. scalaris group, Benabib et al. (1997) mentions and have diurnal habits, and are subject to strong that S. bicanthalis is distributed on the southern side predation pressures that require instant access to cover, of the Transmexican Volcanic Belt, with S. goldmani and use the bunchgrass, rocks, logs, litter and burrows on the north side, and suggest this characteristic may to take refuge. They can be active throughout the year, have evolved independently. However, placement of S. depending on weather conditions (Lemos-Espinal and goldmani in the northern clade was based on isozyme Smith, 2009; Ramírez-Bautista et al., 2009; Canseco- and morphological characters only, because there were Márquez and Gutiérrez-Mayen, 2010; Ramírez- no specimens available to extract DNA. �����������The size of Bautista et al., 2014). These behaviours in other species the litter reported in this study is consistent with that belonging to the S. scalaris group largely coincides reported by Smith and Hall (1974), they found nine with our observations on the behaviour of Sceloporus well-developed embryos in the uterus of the holotype goldmani in its southern distribution. and one paratype of S. goldmani, both from Charcas, San Luis Potosí. Fauna in some category of risk associated with The specimens reported in the note of reproductive Sceloporus goldmani behaviour of S. scalaris in Aguascalientes, Mexico (Carbajal-Márquez et al., 2013), are in fact S. goldmani; Several species of vertebrates in some category of Smith (1937) mentions that S. goldmani is similar in risk in NOM-059-SEMARNAT-2010, share the habitat many ways to S. scalaris, as Thomas and Dixon (1976) with S. goldmani in the new localities. The golden eagle suggested that it is a perfect mimic of S. scalaris, (Aquila chrysaetos) is threatened (A), the peregrine
166 Rubén Alonso Carbajal-Márquez & Gustavo Ernesto Quintero-Díaz 27 TABLE 2. Species of amphibians and reptiles found in the new localities reported here for Sceloporus goldmani.
Table28 2. Species(E = Endemic,of amphibians NE = and No Endemic;reptiles found Pr = Specialin the new Protection, localities A =reported Threatened; here LCfor =Sceloporus Least Concern, goldmani. EN = (E = Endemic, NE = No Endemic; Pr = Special Protection, A = Threatened; LC = Least Concern, EN = Endangered, VU = Vulnerable). 29 Endangered, VU = Vulnerable).
# Class Species Endemism NOM-059-SEMARNAT-2010 IUCN 1 Amphibians Anaxyrus punctatus NE LC 2 Hyla arenicolor NE LC 3 Hyla eximia NE LC 4 Craugastor augusti NE LC 5 Spea multiplicata NE LC 6 Lithobates montezumae E Pr LC 7 Ambystoma velasci NE A LC 8 Reptiles Kinosternon integrum E Pr LC 9 Plestiodon lynxe E Pr LC 10 Aspidocelis gularis NE LC 11 Phrynosoma orbiculare E A LC 12 Holbrookia approximans NE 13 Sceloporus grammicus NE Pr LC 14 Sceloporus minor E LC 15 Sceloporus spinosus E LC 16 Sceloporus torquatus E LC 17 Coluber flagellum NE A LC 18 Coluber mentovarius NE LC 19 Coluber taeniatus NE LC 20 Conopsis nasus E LC 21 Lampropeltis mexicana E LC 22 Pituophis deppei E A LC 23 Salvadora bairdi E Pr LC 24 Tantilla wilcoxi NE LC 25 Trimorphodon tau E LC 26 Hypsiglena jani NE Pr 27 Thamnophis cyrtopsis NE A LC 28 Thamnophis eques NE A LC 29 Thamnophis melanogaster E A EN 30 Thamnophis scaliger E A VU 31 Crotalus aquilus E Pr LC 32 Crotalus molossus NE Pr LC 33 Crotalus scutulatus NE Pr LC 30
falcon (Falco peregrinus) is in special protection (Pr) subject to special protection, eight are2 threatened in as are the black hawk (Buteo albonotatus; Pr), the NOM-059-SEMARNAT-2010; 29 in least concern red-tailed hawk (Buteo jamaicencis; Pr), Swainsoni’s (LC), one vulnerable (VU) and one endangered (EN) in hawk (Buteo swainsoni; Pr), Harris’s hawk (Parabuteo the IUCN Red List (Table 2). unicinctus; Pr), the hawk (Accipiter cooperii; Pr) It is well known that livestock modify the arid among birds, and among mammals the kangaroo rat grasslands, by changing the plant species composition, (Dipodomys phillipsii; Pr) and the shrew (Notiosorex reducing the perennial grass cover, and causing crawfordi; A). In terms of amphibians and reptiles, 33 herpetofauna response to these changes (Jones 1981; species were found; most are typical of the Mexican Bock et al., 1990). For example, Sceloporus slevini Plateau. Of these 15 are endemic to Mexico, nine are (member of S. scalaris group) in south eastern Arizona Natural History of Sceloporus goldmani in its southern distribution 167 shows abundance over 10 times higher in zones to the Sceloporus scalaris species group (Squamata: without grazing in comparison with grazed areas and Phrynosomatidae). Systematic Biology 63: 119-133. for the most part grazed grassland was totally devoid Grummer, J.A., Bryson Jr., R.W. (2014): A new species of bunchgrass lizard (Squamata: Phrynosomatidae) from the of lizards. The S. slevini were concentrated where southern sky islands of the Sierra Madre Occidental, Mexico. numerous intact bunches of Bouteloua curtipendula Zootaxa 3790: 439-450. occurred (Bock et al., 1990). This demonstrates the Jones, K.B. (1981): Effects of grazing on lizards abundance and importance of preserving undisturbed areas in the range diversity in western Arizona. Southwestern Naturalist 26: 107- of Sceloporus goldmani. Due to the several species of 115. vertebrates in some category of risk cohabitating with Leaché, A.D., Palacios, J.A., Minin, V.N., Bryson Jr., R.W. (2013): Sceloporus goldmani we have more reasons that justify Phylogeography of the Trans-Volcanic bunchgrass lizard (Sceloporus bicanthalis) across the highlands of south-eastern the conservation of the habitat, which is being rapidly Mexico. Biological Journal of the Linnean Society 110: 852- transformed into crops and stables and in recent years 865. into wind parks. Lemos-Espinal, J.A., Smith, H.M. (2009): Amphibians and Reptiles of the State of Chihuahua, Mexico. D.F. México, Acknowledgements. We thank Jorge H. Valdez-Villavicencio UNAM, CONABIO, University of Colorado at Boulder. for the pre-peer review of this manuscript. We thank Anny Ramírez-Bautista, A., Hernández-Salinas, U., García-Vázquez, Peralta-García for the comments on a previous version of this U.O., Leyte-Manrique, A., Canseco-Márquez, L. (2009): manuscript. We thank Guillermo Martínez de la Vega, Carolina Herpetofauna del Valle de México: Diversidad y Conservación. Chavez Floriano, Roberto Roque Lozano and Juan Manuel García D.F., México. Universidad Autónoma del Estado de Hidalgo, Alcántara for field support. CONABIO. Ramírez-Bautista, A., Hernández-Salinas, U., Cruz-Elizalde, R., References. Berriozabal-Islas, C., Lara-Tufiño, D., Goyenechea, I., Castillo- Cerón, J. (2014): Los anfibios y reptiles de Hidalgo, México: Aranda, M., López-Rivera N., López-de Buen L. (1995): Hábitos Diversidad, Biogeografía y Conservación. Pachuca, México, alimentarios del coyote (Canis latrans) en la Sierra del Ajusco, Universidad Autónoma del Estado de Hidalgo y Sociedad México. Acta Zoológica Mexicana (n. s.) 65: 89-99. Herpetológica Mexicana A. C. Benabib, M., Kjer, K.M., Sites Jr. J.W. 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(2014): Species delimitation using Bayes factors: simulations and application