DIET OF THE YARROW S SPINY LIZARD SCELOPORUS JARROVII IN THE CENTRAL CHIHUAHUAN DESERT
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1 THE SOUTHWESTERN NATURALIST 56(1):89 94 MARCH 2011 DIET OF THE YARROW S SPINY LIZARD SCELOPORUS JARROVII IN THE CENTRAL CHIHUAHUAN DESERT HÉCTOR GADSDEN,* JOSÉ L. ESTRADA-RODRÍGUEZ, DIANA A. QUEZADA-RIVERA, AND SANDRA V. LEYVA-PACHECO Instituto de Ecología, A.C., Centro Regional Chihuahua, (Cubículo 30C), Miguel de Cervantes 120, Complejo Industrial Chihuahua, C.P , Chihuahua, Chihuahua, México (HG) Centro de Estudios Ecológicos-Escuela Superior de Biología, Universidad Juárez del Estado de Durango, Avenida s/n, Fraccionamiento Filadelfia, Gómez Palacio, Durango, México (JLE-R, DAQ-R, SVL-P) *Correspondent: hector.gadsden@inecol.edu.mx ABSTRACT We studied seasonal dietary patterns of Sceloporus jarrovii from a desert environment northwest of Gomez Palacio, Durango, Mexico. Stomach contents were examined (n 5 82) and relative abundance and volume were determined. Formicids (ants) were the most abundant prey in all seasons. Other abundant foods were coleopterans (summer, winter) and isopterans (autumn, winter). Based on relative abundance in all seasons, S. jarrovii had a narrow breadth of diet, but relative volume of foods was broader. Overlap between sexes for relative abundance and volume was high throughout the year. However, low overlap in relative volume in spring indicated variation in diet between sexes. Three of the most common prey throughout the year varied significantly between sexes in length, width, and volume. However, volumes of the three most abundant foods were not correlated with snout vent length of lizards. RESUMEN Estudiamos los patrones estacionales de la dieta de Sceloporus jarrovii de un ambiente desértico del noroeste de Gómez Palacio, Durango, México. Fueron examinados contenidos estomacales (n 5 82) y se determinó su abundancia y volumen relativo. Los formícidos (hormigas) fueron las presas más abundantes en todas las estaciones. Otros alimentos abundantes fueron los coleópteros (verano e invierno) e isópteros (otoño e invierno). Basados en la abundancia relativa en todas las estaciones, S. jarrovii tenía una amplitud baja de dieta, pero el volumen relativo de alimento fue más alto. El sobrelapamiento entre sexos para abundancia y volumen relativo fue alto a través del año. Sin embargo, el sobrelapamiento bajo de volumen relativo en la primavera indicó variación en dieta entre sexos. Tres de las más comunes presas utilizadas a través del año variaron significativamente entre sexos en longitud, anchura, y volumen. Sin embargo, el volumen de las tres categorías alimentarias más abundantes no estuvo correlacionado con la longitud hocico-cloaca de las lagartijas. Wiens et al. (1999) determined that Sceloporus jarrovii is actually a group of five species (Sceloporus cyanostictus, S. jarrovii, S. minor, S. oberon, and S. sugillatus) that occur in the mountains of southern Arizona, New Mexico, and northwestern Mexico at elevations of 1,370 3,550 m (Stebbins, 2003). Several studies have focused on diet of S. jarrovii (Simon, 1975, 1976; Ballinger and Ballinger, 1979; Simon and Middendorf, 1985; Goldberg and Bursey, 1990; Bursey and Goldberg, 1993). However, these data were collected from populations of S. jarrovii in the United States. In Mexico, data on diet of S. jarrovii do not exist. Ballinger and Ballinger (1979) reported that diet of this lizard was more specialized when food was less abundant. In addition, in the Chihuahuan Desert, seasonal distribution and amount of rainfall appears to be the most important factor affecting availability and abundance of arthropods as food for lizards (Whitford and Creusere, 1977). The purpose of our study was to describe seasonal changes in relative abundance, relative volume, breadth of niche, and overlap in diet of S. jarrovii living in rock crevices in the central Chihuahuan Desert of Mexico. MATERIALS AND METHODS We conducted fieldwork in Las Piedras Encimadas (25u389470N, 103u389400W, 1,425 m elevation), a 10-km long canyon 25 km NW The Southwestern Naturalist swna d 6/1/11 17:21:17 89 Cust # PAS-18
2 90 The Southwestern Naturalist vol. 56, no. 1 Gomez Palacio, Durango, Mexico. Climate of this region is seasonal, with highest temperature and rainfall occurring in spring and summer, respectively. Mean annual temperature was 21uC and mean annual precipitation was 239 mm (Schmidt, 1979). Vegetation was dominated by Agave lechugilla and Jatropha dioica and is in the Lechuguilla Scrub plant community (Rzedowsky, 1978). Sympatric lizards in the study area were Aspidoscelis septemvittata, Cophosaurus texanus, and Sceloporus poinsettii. Throughout the study site, rock faces with crevices, an important microhabitat for S. jarrovii, were numerous. A total of 82 specimens (40 males, 42 females) of adult S. jarrovii was noosed or shot with BB rifles during monthly sampling in April 2004 March 2005 ( individuals/month). Because of seasonal similarities in temperature and precipitation, we pooled monthly samples for each season (winter, January March; spring, April June; summer, July September; autumn, October December). We collected lizards during 1,000 1,400 h with equal sampling effort throughout this period. Immediately following capture, lizards were measured and weighed, placed on ice, and subsequently frozen and preserved in 10% formalin (Gadsden and Palacios-Orona, 1997; Gadsden et al., 2001). We deposited specimens in the collection of the Universidad Juárez del Estado de Durango (voucher specimens-ujed-esb-sj-1-82). In the laboratory, we removed stomach contents, and spread food items in a Petri dish. Prey were identified to order or family, and length and width were measured using an optical micrometer. Later, we estimated individual volumes of food using the formula for a prolate spheroid (Vitt and Morato de Carvalho, 1992). We measured relative abundance (average percentage of number of food items per stomach) and relative volume of food (percentage of total volume of food). Breadth of food niche was determined in two ways, using Shannon-Wiener s index (H9 52Sp i log 2 p i ). First, p i was designated as the proportion of prey items in the gastrointestinal tract in the i th prey category. The probability that any one individual belongs to preycategory i is p i. Trophic diversity is greatest if each individual prey belongs to a different category. Trophic diversity is lowest if all individuals belong to one category. For the other analysis (H v ), p i was designed as the proportion of the total volume of prey in the gastrointestinal tract occupied by individuals in the i th prey category (Pianka, 1973; Barbault et al., 1978). Because the Shannon-Wiener s measure can range from 0 to, both estimates of breadth of niche were standardized to a 0.0 to 1.0 scale by dividing by H max (maximum value of H9 and H9 v ; Krebs, 1999). We measured overlap between sexes using an index developed by Pianka (1975): Ojk ~ S p ij p ik qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi S p ij 2 S p ik 2 where p ij and p ik represent the proportions of prey belonging to the i th category that were used by the j th and k th organism, respectively. Overlap ranges from 0 (no overlap) to 1 (complete overlap). This measure requires that all prey in the microhabitat of S. jarrovii are equally available to both sexes. Ricklefs and Lau (1980) demonstrated that sampling distributions of all measures of overlap in niche are strongly affected by size of sample. Also, Smith and Zaret (1982) reported that bias increases in all measures of overlap as number of resource categories increase. Bias can be quite large when number of resource categories is large, even if samples are reasonably large. Bias is minimized when both sexes are sampled equally (Krebs, 1999). We calculated sample means (6SE) for three morphometric characteristics (length, width, and volume) of insect prey and Mann-Whitney U-tests were used to test for significant differences in diet between sexes. We examined the relationship between volume of prey and snout vent length of lizard for the main insect prey using Pearson s correlation analysis. All statistical analyses were performed with SPSS base 8.0 (1998). RESULTS The 82 stomachs yielded 1,455 individual food items (737 for males, 718 for females). There were eight types of food in stomachs during the year; only three groups were dominant for relative abundance and relative volume: hymenopterans (all were formicids; annual mean % and %, respectively), isopterans (annual mean % and %, respectively), and coleopterans (annual mean % and %, respectively; Tables 1 and 2). Formicids and coleopterans were consistently abundant in stomachs (Table 1). In autumn, isopterans also were abundant and orthopterans and arachnids were moderately abundant during spring. Relative volumes of food items (Table 2) changed among seasons, e.g., isopterans had a large increase in autumn. However, formicids were abundant during all seasons. There were sexual differences in spring (relative volume, x , P, 0.01); males ate arachnids (64.1%) and a smaller volume of formicids (16.1%), whereas females primarily consumed formicids (85.2%) and coleopterans (9.2%; Table 2). Likewise in summer, males consumed more diverse foods than females (relative volume, x , P, 0.01), increasing considerably the frequency of coleopterans (30.1%) and homopterans (16.1%) in the diet. Diet of S. jarrovii abruptly shifted in autumn, with considerable increase in isopterans and decrease in formicids (Tables 1 and 2). This shift was coincident with the decrease in precipitation in 2004 after early autumn (concentrated during summer and early autumn; Gadsden and Estrada-Rodríguez, 2008). Shannon-Wiener s indi- The Southwestern Naturalist swna d 6/1/11 17:21:17 90 Cust # PAS-18
3 March 2011 Gadsden et al. Diet of Yarrow s spiny lizard 91 TABLE 1 Seasonal relative abundance of food items in stomachs (average percentage) of adult male and female Sceloporus jarrovii from Durango, Mexico ( ). Food item Spring Summer Autumn Winter Males Females Males Females Males Females Males Females n 5 9 n 5 10 n 5 11 n 5 12 n 5 12 n 5 13 n 5 8 n 5 7 Total number Coleoptera Hemiptera Homoptera Isoptera Formicidae ,313 Diptera Orthoptera Araneae Number of individuals ,455 ces (Table 3) indicated narrow breadth of niche for relative abundance (H9, 0.41); relative volume was broader (H9.0.50). In general, annual overlap in diet between sexes for relative abundance (O jk 6 SD) and relative volume (O jk 6 SD) was high (O jk and O jk ). Low volumetric overlap in spring (O jk ) indicated a difference in diet between sexes. Snout vent length of adult males was mm (mean 6 1 SE, n 5 43), which was significantly larger than snout vent length of adult females (mean mm, n 5 51; Mann-Whitney U-test, Z , P, 0.001). Two of the most common foods (coleopterans and isopterans) varied significantly between sexes in length, width, and volume (Table 4). However, volumes of the three most common foods were not correlated with snout vent length (formicids: r , P. 0.05, n 5 39; coleopterans: r , P. 0.05, n 5 18; isopterans: r , P. 0.05, n 5 17, respectively). DISCUSSION Formicids and coleopterans were the most consistently abundant prey. However, diet of S. jarrovii abruptly shifted in autumn, with isopterans increasing considerably and formicids decreasing. In the central Chihuahuan Desert, Maury (1995) reported that fluctuation in diversity and abundance of prey in Cophosaurus texanus was correlated with effect of precipitation on primary productivity. Rainfall was also an important factor in emergence from diapause of some coleopterans, formicids, and dipterans, and an increase of breeding activity in formicids and isopterans (Maury, 1995). According to TABLE 2 Seasonal changes in relative volume of food in stomachs (percentage of total volume of food) of adult male and female Sceloporus jarrovii from Durango, Mexico ( ). Food item Spring Summer Autumn Winter Males Females Males Females Males Females Malea Females n 5 9 n 5 10 n 5 11 n 5 12 n 5 12 n 5 13 n 5 8 n 5 7 Total volume (mm 3 ) Coleoptera Hemiptera Homoptera Isoptera Formicidae ,860 Diptera Orthoptera Araneae ,371 Total volume (mm 3 ) 2, , ,373 The Southwestern Naturalist swna d 6/1/11 17:21:17 91 Cust # PAS-18
4 92 The Southwestern Naturalist vol. 56, no. 1 TABLE 3 Shannon-Wiener s indices of food items in stomachs of adult Sceloporus jarrovii from Durango, Mexico ( ) by season. Realtive abundance H9 Relative volume H9v Season Males Females Males Females Spring Summer Autumn Winter Ballinger and Ballinger (1979), seasonal differences in environmental conditions, such as precipitation, appear to regulate diversity and abundance of foods, and thereby indirectly influence changes in diet of some lizards. As in other populations of S. jarrovii in the United States (Simon, 1975; Ballinger and Ballinger, 1979), the population we studied was estimated to have narrow breadth of diet coincident with low precipitation during According to Ballinger and Ballinger (1979), S. jarrovii is forced to take large numbers of small food items during low-resource years and simply consumes more of these items because of the small sizes of prey. If this is true, then diversity indices of foods taken should be lower in poorresource years. The large numbers of formicids would be consumed largely because these insects often are smaller than insects such as coleopterans. Thus, for a lizard to gain equal amounts of energy from formicids and coleopterans, substantially more formicids need to be consumed. The high overlap in diet between sexes suggests that males and females may forage in the same area or possibly is evidence that insects occur in relatively equal abundance across the area. Both sexes use the same crevice-dwelling habit (Gadsden and Estrada-Rodríguez, 2007) and they also have the same foraging areas. Peak foraging activity occurs at ca. 1,000 1,300 h in both sexes (Smith and Ballinger, 1994). Simon (1975, 1976) reported that male and female S. jarrovii maintain overlapping territories during all months of activity, whereas male-male and female-female overlaps rarely occur. Consequently, foods used by both sexes were similar during all seasons. Nevertheless, foraging ecology for S. jarrovii must be studied in greater detail to explain the apparent volumetric differences in diet between sexes during spring (season with many gravid females; Gadsden and Estrada- Rodríguez, 2008). A probable factor that influences this exclusive difference in volume between sexes in spring is the different energetic requirements of gravid females compared to males and non-gravid females. Also, females carrying near or full-term eggs might forage shorter distances than males, and this might explain the different volume in diet between sexes in spring (Simon, 1975; Simon and Middendorf, 1976). However, winter (with most gravid females; Gadsden and Estrada-Rodríguez, TABLE 4 Statistical comparison of morphometric characteristics (annual means 6 SE; n in parentheses) of main food items in stomachs of adult Sceloporus jarrovii from Durango, Mexico. Statistical test is Mann-Whitney U (P, *), and ns 5 not significant. Parameter/food item Males Females Z Length of prey (mm) Coleoptera (12) (23) 23.4* Formicidae (371) (334) 27.1* Isoptera (21) (44) 25.3* Width of prey (mm) Coleoptera (12) (23) 24.2* Formicidae (371) (334) 1.4ns Isoptera (21) (44) 27.8* Volume of prey (mm 3 ) Coleoptera (12) (23) 24.2* Formicidae (371) (334) 26.6* Isoptera (21) (44) 27.3* The Southwestern Naturalist swna d 6/1/11 17:21:19 92 Cust # PAS-18
5 March 2011 Gadsden et al. Diet of Yarrow s spiny lizard ) showed a high volumetric overlap in diet between sexes. Although diets of male and female S. jarrovii are similar, differences in diet may reflect prey items in that portion of the habitat occupied by, or available to, a specific sex during its activity period or may represent prey most easily caught and ingested (Bursey and Goldberg, 1993). Ruby (1978) reported that home ranges of adult male S. jarrovii always were larger than those of adult females. This may have exposed males and females to different foraging opportunities. Also, perch site is correlated with size; small S. jarrovii tended to perch near the ground, while larger lizards had higher locations (Simon and Middendorf, 1976). This could have denied females access to potential prey that occurred above ground level. Finally, male S. jarrovii have significantly greater width and length of head than females (Gadsden and Estrada-Rodríguez, 2007). Thus, gape might have restricted size of prey more for females than males. Sexual dimorphism in S. jarrovii, as in other species of the genus, usually is attributed to sexual selection when males are the larger sex (Fitch, 1981; Stamps, 1983; Shine, 1989). Diet of S. jarrovii in our study differed in relative abundance, relative volume, and taxonomic composition from that reported for S. jarrovii by Ballinger and Ballinger (1979), primarily because of the importance of termites in autumn and winter. Termites are significant components in diets of other Sceloporus in Mexico. Gadsden and Palacios-Orona (1995) noted that termites were a significant component of the diet of S. undulatus from northeastern Durango, with formicids, coleopterans, and lepidopteran larvae also being important. Termites also made up a substantial portion of the diets of S. clarki and S. nelsoni in Sonora (Brooks and Mitchell, 1989). The degree of vertebrate termitivory is highest in semi-arid and arid biomes (Abensperg-Traun, 1994). Our study revealed that diet shifted to increased consumption of isopterans in autumn. However, prey such as formicids and coleopterans consistently were abundant throughout all seasons. Variation in feeding biology in the population we studied might reflect adaptations to variability of feeding resources in a highly unpredictable environment. A quantitative comparison of selection of prey and abundance of insects before and after rains is planned and should elucidate feeding strategies. This study was supported by a grant (43142-Q) from Secretaría de Educación Pública-Consejo Nacional de Ciencia y Tecnología. We thank O. Hinojosa de la Garza for providing support and encouragement to HG throughout analyses of data. Research was conducted under permit Secretaría de Medio Ambiente y Recursos Naturales-Subsecretaría de Gestión para la Protección Ambiental/Dirección General de Vida Silvestre/ LITERATURE CITED ABENSPERG-TRAUN, M The influence of climate on patterns of termite eating in Australian mammals and lizards. Australian Journal of Ecology 19: BALLINGER, R. E., AND R. A. BALLINGER Food resources during periods of low and high food availability in Sceloporus jarrovi (Sauria: Iguanidae). Southwestern Naturalist 24: BARBAULT, R., C. GRENOT, AND Z. URIBE Le partage des ressources alimentaires entre les espéces de lézards du desert de Mapimí (Mexique). La Terre et la Vie 32: BROOKS, G. R., AND J. C. MITCHELL Predator-prey size relations in three species of lizards from Sonora, Mexico. Southwestern Naturalist 34: BURSEY, C. R., AND S. R. GOLDBERG Diet of neonatal Yarrow s spiny lizard, Sceloporus jarrovii jarrovii (Phrynosomatidae). Southwestern Naturalist 38: FITCH, H. S Sexual size differences in reptiles. Miscellaneous Publications, Museum of Natural History, University of Kansas 70:1 72. GADSDEN, H. E., AND J. L. ESTRADA-RODRÍGUEZ Ecology of the spiny lizard Sceloporus jarrovii in the central Chihuahuan Desert. Southwestern Naturalist 52: GADSDEN, H. E., AND J. L. ESTRADA-RODRÍGUEZ Demography of the Yarrow s spiny lizard, Sceloporus jarrovii from the central Chihuahuan Desert. Western North American Naturalist 68: GADSDEN, H. E., AND L. E. PALACIOS-ORONA Variación de la alimentación de Sceloporus undulatus (Reptilia: Phrynosomatidae) en el Bolsón de Mapimí, México. Boletín de la Sociedad Herpetológica Mexicana 6: GADSDEN, H. E., AND L. E. PALACIOS-ORONA Seasonal dietary patterns of the Mexican fringetoed lizard (Uma paraphygas). Journal of Herpetology 31:1 9. GADSDEN, H. E., L. E. PALACIOS-ORONA, AND G. CRUZ-SOTO Diet of the Mexican fringe-toed lizard (Uma exsul). Journal of Herpetology 35: GOLDBERG, S. R., AND C. R. BURSEY Winter feeding in the mountain spiny lizard, Sceloporus jarrovi (Iguanidae). Journal of Herpetology 24: The Southwestern Naturalist swna d 6/1/11 17:21:19 93 Cust # PAS-18
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