Size- and Sex-Dependent Variation in Diet of Rhinella Arenarum (Anura: Bufonidae) in a Wetland of San Juan, Argentina

Size- and Sex-Dependent Variation in Diet of Rhinella arenarum (Anura: Bufonidae) in a Wetland of San Juan, Argentina

Authors: Quiroga, Lorena B., Sanabria, Eduardo A., and Acosta, Juan C. Source: Journal of Herpetology, 43(2) : 311-317 Published By: Society for the Study of Amphibians and Reptiles URL: https://doi.org/10.1670/07-117R2.1

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Size- and Sex-Dependent Variation in Diet of Rhinella arenarum (Anura: Bufonidae) in a Wetland of San Juan, Argentina

1 LORENA B. QUIROGA, EDUARDO A. SANABRIA, AND JUAN C. ACOSTA

Departamento de Biologı´a, Instituto y Museo de Ciencias Naturales, Universidad Nacional de San Juan, Avenida Ignacio de la Roza 590 (O), Co´digo Postal:5400, Argentina

ABSTRACT.—We studied body-size and sex-dependent variation in the diet of Rhinella arenarum in a wetland of San Juan, Argentina. We hypothesized that prey size would be positively correlated with toad size and that the guts of larger toads would contain fewer prey items. Toads from this population eat primarily ants and, secondarily, beetles, indicating a feeding strategy that is intermediate between specialist and generalist. This feeding strategy may be influenced by prey availability. Contrary to our expectation, prey size was not related to toad body size, and the relationship between the prey number and toad body size was positive. Our findings, coupled with similar diet studies of toads, suggest geographically widespread phylogenetic conservatism in the diet of bufonids.

Both extrinsic factors, such as seasonal food remain dry (Victoria, 1999). The region belongs to the abundance and the presence of competitors and Monte phytogeographic province, which has an arid predators, and intrinsic factors, such as morphological climate and a mean annual temperature of 17.3uC, a constraints resulting from ontogeny, body size, and mean maximum annual temperature of 25.7uC, a specialization (Toft, 1980; Duellman and Trueb, 1986) mean minimum annual temperature of 10.4uC, and a influence an amphibian’s diet. For example, the size of mean annual rainfall of 89 mm, which falls mainly in a frog (or its gape) is often a good predictor of the size summer (Cabrera, 1994). The dominant plants of this of prey it will take. However, larger individuals tend Monte region include Cortaderia sp., Typha dominguen- to consume prey of a wider range of body sizes (Toft, sis, Malvella leprosa, Phyla canescens, Melilotus indicus, 1980; Hirai and Matsui, 1999, 2000, 2002b; Menendez- Gnaphalium sp., Cyperus sp., Prosopis strombulifera, Guerrero, 2001; Hirai, 2002). Prosopis sp., Atriplex sp., and Larrea spp. We studied the diet of a population of the common Toads were collected from 28 November 2001 to 5 toad Rhinella arenarum, in an arid region of San Juan, October 2002, except during winter (May to July), Argentina. Rhinella arenarum is widely distributed in when the animals are not active. A total of 149 Argentina from northern Jujuy Province to the Rı´o individuals was haphazardly collected during day- Chubut in Patagonia. Despite being one of the most and nighttime visual-encounter surveys (Heyer et al., common anurans in this region, most aspects of the 2001), which took place approximately every 10 days ecology of this toad are not well known (Cei, 1980; during the sampling period. Specimens were imme- Gallardo, 1987). Bufonids are widely considered diately sacrificed, fixed in 10% formalin, and pre- generalist predators (Lajmanovich, 1995; Parmelee, served in 70% alcohol. Body length (snout–vent 1999; Hirai and Matsui, 2002b; Moseley et al., 2005). length; SVL) and mouth width (MW) were measured However, most of the toads studied to date eat with digital calipers (0.01 mm precision) and mass primarily beetles and ants, the latter of which can be with a digital balance (Denver Pk-1201; 0.1 g preci- ingested in large quantities because of their often- sion). Sex was determined by dissection; postmeta- clumped distribution (Menendez-Guerrero, 2001). morphic, yet sexually immature individuals were R. arenarum Our objective was to analyze the diet of , considered subadults up to 8 cm. providing basic information on the biology of this Stomachs were excised between the cardiac and widespread species. We predicted that larger R. pyloric sphincters, and their contents were analyzed arenarum from our population would eat larger and under a binocular dissecting microscope (3 2–40). The a wider of range prey items than would smaller length and width of each prey item was measured individuals. Specifically, we hypothesized that (1) prey size would increase with toad size and that (2) with digital calipers and prey volume was estimated 5 p 2 the number of prey would decrease with the size of using the equation [V 4/3 (L/2) (W/2) ] for an the toad. elliptical sphere (Dunham, 1983). Prey items were classified to the lowest taxonomic level allowed by MATERIALS AND METHODS their state of digestion. We studied a population of R. arenarum from a The percentage of plant tissues was estimated with seasonal wetland produced by the Ullu´m Reservoir respect to the total amount of food. An index of 25 km west of San Juan, Departamento Zonda, relative importance (IRI 5 %FO [%N + %V] [Pinkas et Provincia de San Juan, Argentina (31u559S, 68u709W; al., 1971]) was used to compare the dietary contribu- 800 m). The wetland has uneven terrain, with the tion of each food category; where %FO is the lower areas flooding in summer, while higher areas frequency of occurrence of food category, %N is the numerical percentage, and %V the volumetric percentage, of the analysis toad. A dietary hierarchy (DH) 1 Corresponding Author. E-mail: quiroga_lore@ was obtained by adding the IRI of each order yahoo.com.ar contribute, and then the percentage was calculated

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TABLE 1. Diet composition of Rhinella arenarum by size class. Abbreviations: N, number of prey; IRI, index of relative importance; DH, dietary hierarchy; Ni, not identified. The sum of the IRI for each taxonomic category is in bold.

Adults Subadult Prey category N IRI DH N IRI DH VERTEBRATA Squamata Leptotyphlopidae 2 0.08 0.004 Rodentia Mus musculus 1 0.34 0.02 INSECTA Coleoptera 612.92 36.4 155.52 5.50 Curculionidae 459 231.90 6 67.22 Coccinellidae 23 1.24 Cicindelidae 17 3.44 Cerambycidae 2 0.12 Carabidae 302 343.55 5 35.07 Elateridae 50 7.82 Lampyridae 7 0.31 Larvae 6 0.50 3 3.01 Meloidae 2 0.03 Scarabaeidae 54 23.49 2 48.86 Scolytidae 1 0.01 Ni 7 0.51 2 1.36 Orthoptera 11.17 0.6 10.9 0.38 Gryllotalpidae S. borellii 1 0.02 Acrididae 4 0.58 1 5.35 Gryllidae 17 10.57 1 4.74 Thysanoptera Thrips 2 1.27 0.04 Blattaria 0.22 0.01 Blattidae 2 0.10 Ootheca-P. americana 1 0.01 Philodromidae 2 0.11 Diptera 0.74 0.04 21.84 0.77 Larvae 1 0.01 Culicidae 31 0.71 16 19.14 Calliphoridae Calliphora sp. 1 0.01 4 2.40 Ni 2 0.01 1 0.30 Dictyoptera Mantidae 1 0.32 0.01 Hemiptera 1.29 0.07 5.17 0.18 Belostomatidae 1 0.04 1 1.51 Notonectidae 1 0.07 Pentatomidae 5 0.58 Ni 4 0.09 4 3.66 Homoptera 11 0.51 0.03 27 7.97 0.28 Hymenoptera 1,679.66 100 2,824.15 100 Pupae 1 0.01 Apidae 7 1.27 Formicidae 5,248 1,677.53 99.87 455 2,823.56 99.97 Sphecidae 1 0.02 Vespidae 13 0.83 1 0.59 Isoptera 260 2.72 0.1 2 0.59 0.02 Lepidoptera 0.74 0.04 0.89 0.03 Ni 4 0.04 1 0.30 Larvae 5 0.44 2 0.59 Pupae 5 0.26 ARACHNIDA Acarii 1 0.002 0.0001 29 50.99 1.80

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TABLE 1. Continued.

Adults Subadult Prey category N IRI DH N IRI DH Aranae 6.79 0.4 Aracnidae 36 6.76 1 0.62 0.02 Solifugae 1 0.03 CRUSTACEA Isopoda 1,002 349.30 18 56 178.55 6.32 ANNELIDA Oligochaeta Haplotaxidae 2 0.01 0.0005 MYRIAPODA 2 0.01 0.0005 1 0.34 0.01 OTHERS 2 0.88 0.05 TOTAL 7,608 623

that contributed each order to the diet. Prey were RESULTS considered fundamental if its percentage was between 100% and 75%, secondary if it was between 74% and A total of 149 stomachs was analyzed: 20 were 50%, accessory if was between 49% and 25%, and rare empty; and of those containing prey items, 19 were subadults and 110 adults (41 females and 69 males). if it was below 25% (Montori, 1991). P ~ n 2 The stomachs of R. arenarum from this San Juan The trophic niche breadth (Nb 1 i ~ 1 Pi )of each size class and sex was defined using Levins’s population included 8,231 prey items, which were index (Levins, 1968); where i is the resource category, assigned to 48 taxa (Table 1). The trophic niche breadth P is the proportion of resource category i, and n is the value for all individuals was Nb 5 2. Females were total number of categories. Trophic niche breadth larger than males, and both were larger than subadults; values range from 1 (use of only one type of prey) to n females also had more prey items than males, and both (all prey types used equally). had more than subadults (Table 2). The ANCOVA Jaccard’s similarity index, which measures similar- (with SVL as the covariate) failed to detect differences ity between qualitative variables, was used to test for between the size classes in the number of prey and relationships between dietary size classes and sexes MPV (F1,105 5 0.03–0.69; P 5 0.32–0.84). (Moreno, 2001). To measure the similarities between Among adults of both sexes, Formicidae (ants) were size classes and sexes in quantitative variables (IRI, the most numerous prey item (68.7%), followed by prey number, and prey volume) we used the Spear- Isopoda (isopods; 12.9%) and Coleoptera (beetles; man’s correlation test. We used ANCOVA (with SVL 12.4%). Beetles were volumetrically the most impor- as the covariate) to analyze the differences between tant group (46.0% vs. 20.8% for ants), although the IRI size classes. was greater for ants (IRI 5 1,677.5) than for beetles

TABLE 2. Morphometric measures (mean 6 SE [range]) and mean volume of prey consumed, as well as other feeding characteristics of each age group. Abbreviations: SVL, snout–vent length; MW, mouth width; TNB, trophic niche breadth.

Adult Size classes Males Females Subadult Number of individuals 110 19 69 41 SVL 96.1 6 0.85 (30) 110.3 6 1.47 (38.4) 35.5 6 6.08 (69.2) MW 35.8 6 0.28 (10) 40.1 6 0.44 (10) 13 6 2.45 (28) No. of prey in stomach 7,608 623 3,291 4,317 Mean prey number 69.16 35.11 47.7 105.3 Mean prey volume 303.4 6 271.5 (1,621.3) 391.2 6 191.8 (3,950.1) TNB 2.43 1.73 0.88 Trophic spectrum 37 36 23

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FIG. 1. Index of relative importance (IRI) of prey consumed by adult Rhinella arenarum; %Number represents the numerical percentage, %Volume, the volumetric percentage, and the horizontal axis represents the frequency of occurrence of each item.

(IRI 5 612.9; Fig. 1). The diet hierarchy for adult R. DISCUSSION arenarum found ants to be a fundamental item, beetles The population of R. arenarum we studied in San an accessory item, and isopods as the most important Juan primarily eats ants, which were the principal rare item (Fig. 2). diet item in both adults and subadults, followed by Among subadults, ants constituted the highest Coleoptera as the most important accessory item. percentages in both prey number (73.0%) and volume This finding is similar to those described for other (46.2%). Similarly, the IRI was once again highest for ants (IRI 5 2818; Fig. 3). Ants appeared as a toad species (e.g., Epidalea calamita,Lo´pez Jurado, fundamental item in the dietary hierarchy, but there 1982; R. arenarum, Rhinella schneideri, and Rhinella were no secondary or accessory items; Isopoda, fernandezae, Lajmanovich, 1995; Rhinella margaritifera Coleoptera, Acari, Aranae, and Diptera appeared as and Rhinella marina, Mene´ndez-Guerrero, 2001; Bufo rare items (Fig. 2). japonicus formosus, Hirai and Matsui, 2002a; R. The correlation between predator size (all individ- schneideri,Lo´pez, 2003; Anaxyrus terrestris, Moseley uals; SVL and MW) and prey size (mean prey volume, et al., 2005). MPV) was significant in every case (Table 3). The Parmelee (1999) suggested that all bufonids have body size variables (SVL and MW) for adults were not similar diets. Ants and coleopterans are the most correlated with MPV, whereas the size variables for numerous prey, but a variety of other small prey are subadults were positively correlated with MPV also eaten. The diet of R. arenarum may be influenced (Table 3). by prey availability, as in other studies (Guix, 1993), Jaccard’s similarity index comparing adults and but we did not attempt to quantify this. The high subadults was 0.63, and the value comparing males frequency of ant eating suggests that R. arenarum takes and females was 0.60. Spearman’s correlation between advantage of the availability of this often-clumped size classes (adults vs. subadults) was significant for resource, which moves slowly and, although low in IRI (r 5 0.71; P , 0.001; N 5 21), and prey volume (r 5 energy and nutrients, can be ingested in large 0.52; P 5 0.02; N 5 21), and prey number (r 5 0.76; P quantities (Menendez-Guerrero, 2001). The high val- , 0.001; N 5 21), and sexes for IRI (r 5 0.65; P 5 0.02; ues of IRI are attributable to the numerical fraction of N 5 38), and prey volume (r 5 0.51; P 5 0.02; N 5 38), ants rather than their volumetric fraction (see also and prey number (r 5 0.85; P , 0.001; N 5 38). Basso, 1990). The proportional number of ants in the

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FIG. 2. Diet hierarchy (DH) using the rating system of Montori (1991) of the index of relative importance for adult and subadult Rhinella arenarum.

diet of R. arenarum was high for both size classes, in example, an Andean population of R. spinulosa was agreement with Parmelee (1999) who suggested that reported to consume a large amount of plants because most bufonids consume large quantities of relatively of a lack of animal prey (Nu´n˜ ez et al., 1982). small prey. Observations suggest that this is consistent with the Because most toads eat a wide variety of prey items conclusion that R. arenarum incidentally ingests plant and wait for prey to approach them rather than material while consuming foraging ants. actively forage for their meals, they are generally Our regression analyses show that, as predator size considered to have a ‘‘sit-and-wait’’ feeding strategy increases, thus does prey size, which is consistent with (Duellman and Trueb, 1986). However, the selection of the results of other studies on anurans that examined large quantities of a few prey items, as was the case predator-prey size relationships (Caldwell and Vitt, for the toads in our study, indicates that some 1999; Menendez-Guerrero, 2001; Hirai, 2002; Maneyro bufonids might better be classified as specialists. et al., 2004). However, ANCOVAs failed to detect Because we lack data on prey availability, we differences between size classes independent of body tentatively consider the R. arenarum population we size. The relationship between the number prey and studied as having an intermediate feeding strategy, as toad body is not negative as we hypothesized. reported for several Argentine anurans (e.g., Dendrop- The heads of this species are not strongly sexually sophus sanborni, Scinax squalirostris, and Pseudopaludi- dimorphic (Quiroga et al., 2004), and they share the cola falcipes, Basso, 1990; R. arenarum and R. schneideri, same microhabitat use (Sanabria et al., 2005). As a Lajmanovich, 1995; and R. schneideri, M. Dure´ and A. result, the similarity between diets of adult males and Kher, unpubl. data). females was also high when they eat the same foods. The high frequency of plant tissues encountered in Our general findings for this primarily ant-eating the stomachs could result from adhesion of prey, and species are similar to those reported for other the plants that they associate with, to the toads’ sticky bufonids in different areas of the world (e.g., Toft, tongue, as was proposed for E. calamita (Lo´pez Jurado, 1980; Guix, 1993; Lajmanovich, 1994; Moseley et al., 1982). Alternatively, the presence of plant tissues 2005), suggesting that the diets of bufonids may be could be explained as by products of the ingestion of widely phylogenetically conserved. leaf-cutting ants (Lajmanovich, 1994). Another expla- nation that is less commonly invoked is that the toads Acknowledgments.—We thank to R. Espinoza for his purposefully ingest plants, a rare but increasingly comments and English review and anonymous recognized feeding strategy for adult anurans. For reviewers for their comments.

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FIG. 3. Index of relative importance (IRI) of prey consumed by subadult Rhinella arenarum; %Number represents the numerical percentage, %Volume, the volumetric percentage, and the horizontal axis represents the frequency of occurrence of each item.

TABLE 3. Correlations between predator and prey DUNHAM, A. E. 1983. Realized niche overlap, resource body size for all toad and separated by size classes. abundance and intensity of interspecific competi- Abbreviations: SVL, snout–vent length; MW, mouth tion. In R. B. Huey, E. R. Pianka, and T. W. width; MPV, mean prey volume. Schoener (eds.), Lizard Ecology, pp. 261–280. Harvard University Press, London. ALLARDO ´ Predator Prey All individuals Adults Subadults G , J. M. 1987. Anfibios Argentinos. Guıa para su Identificacioń. Biblioteca Mosaico. Buenos 2 2 SVL vs. MPV r 5 0.12 — r 5 0.39 Aires, Argentina. P , 0.0001 P 5 0.9 P 5 0.005 GIUX, J. C. 1993. Ha´bitat y alimentaciońdeBufo 2 MW vs. MPV r 5 0.12 — r2 5 0.37 paracnemis en una regioń semia´rida del nordeste P , 0.0001 P 5 0.74 P 5 0.007 de Brasil, durante el perıódo de reproduccioń. Revista Espan˜ ola de Herpetologıá 7:65–73. HEYER, R. W., M. A. DONNELLY,R.W.MCDIARMID,L.C. LITERATURE CITED HAYEK, AND M. S. FOSTER. 2001. Mediciońy Monitoreo de la Diversidad Biolo´gica, Me´todos BASSO, N. G. 1990. Estrategias adaptativas en una Estandarizados para Anfibios. Editorial Universi- comunidad subtropical de anuros. Serie Mono- taria de la Patagonia, Patagonia, Argentina. grafıás No. 1. Cuadernos de Herpetologıá 70 San HIRAI, T. 2002. Ontogenetic change in the diet of the Miguel de Tucumań, Argentina. pond frog, Rana nigromaculata. Ecological Research CABRERA, A. L. 1994. Enciclopedia Argentina de 17:639–644. Agricultura y Jardinerıá. Editorial ACME S.A.C.I., HIRAI, T., AND M. MATSUI. 1999. Feeding habits of the Buenos Aires, Argentina. pond frog, Rana nigromaculata, inhabiting rice CALDWELL, J. P., AND L. J. VITT. 1999. Dietary asymmetry fields in Kyoto, Japan. Copeia 1999:940–947. in leaf litter frogs and lizards in a transitional ———. 2000. Myrmecophagy in a ranid frog Rana northern Amazonian rain forest. Oikos 84:383–397. rugosa: specialization or weak avoidance to ant CEI, J. M. 1980. Amphibians of Argentina. Monitore eating. Zoological Science 17:459–466. Zoologico Italiano. Monografie 2:1–609. ———. 2002a. Feeding ecology of Bufo japonicus DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of formosus from the montane region of Kyoto, Japan. Amphibians. McGraw-Hill, New York. Journal of Herpetology 36:662–667.

Downloaded From: https://bioone.org/journals/Journal-of-Herpetology on 12 May 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by Bing Search Engine SHORTER COMMUNICATIONS 317

———. 2002b. Feeding relationships between Hyla MOSELEY, K. R., S. B. CASTLEBERRY,J.L.HANULA, AND W. japonica and Rana nigromaculata in rice fields of M. FORD. 2005. Diet of southern toads (Bufo Japan. Journal of Herpetology 36:719–723. terrestris) in Loblolly Pine (Pinus taeda) stands LAJMANOVICH, R. C. 1994. Ha´bitos alimentarios de Bufo subject to coarse woody debris manipulations. paracnemis (Amphibia, Bufonidae) en el Parana´ America Midland Naturalist 153:327–337. medio, Argentina. Revista Hydrobiologica Tropi- NU´ N˜ EZ, H., M. A. LABRA, AND J. YAN˜ EZ. 1982. Ha´bitos cal 27:107–112. alimentarios de dos poblaciones andinas de Bufo ———. 1995. Relaciones tro´ficas de bufonidos en spinulosus Wiegmann. Boletıń Museo Nacional de ambientes del Rıó de la Parana´, Argentina. Alytes Historia Natural, Chile 39:81–91. 13:87–103. PARMELEE, J. R. 1999. Trophic ecology of a tropical LEVINS, R. 1968. Evolution in Changing Environments. anuran assemblage. Scientific Papers. Natural Princeton University Press, Princeton, NJ. History Museum, University of Kansas 11:1–59. LO´ PEZ, J. A. 2003. Ecologıá tro´fica de una comunidad PINKAS, L., M. S. OLIPHANT, AND Z. L. IVERSON. 1971. de anuros en un remanente forestal asociado al rıó Food habits of Albacore Bluefin, tuna and Bonito Parana´ Medio. Unpubl. thesis, Universidad Nacio- in California waters. California Department Fish naldelLitoralFacultaddeHumanidadesy Game, Fish Bulletin 152:1–350. Ciencia, Argentina. QUIROGA, L. B., E. A. SANABRIA, AND J. C. ACOSTA. 2004. LO´ PEZ-JURADO, L. F. 1982. Estudios sobre el sapo Dimorfismo sexual en una poblaciońdeBufo corredor (Bufo calamita) en el sur de Espan˜ a. arenarum (Anura: Bufonidae) en los humedales Don˜ ana, Acta Vertebrata 9:71–84. de Zonda, San Juan, Argentina. Boletıńdela MANEYRO, R., D. E. NAYA,I.DA ROSA,A.CANAVERO, AND Sociedad Herpetolo´gica Mexicana 12(2):37–42. A. CAMARGO. 2004. Diet of the South American frog SANABRIA, E. A., L. B. QUIROGA, AND J. C. ACOSTA. 2005. Leptodactylus ocellatus (Anura, Leptodactylidae) in Patrones de actividad temporal estacional y uso de Uruguay. Iheringia, Porto Alegre 94:57–61. microha´bitat de una poblacioń de adultos de Bufo MENE´ NDEZ-GUERRERO, P. A. 2001. Ecologıá tro´fica de la arenarum, en los humedales de Zonda, San Juan, comunidad de anuros del Parque Nacional Yasunı´ Argentina. Boletıń de la Sociedad Herpetolo´gica en la Amazonia Ecuatoriana. Unpubl. Thesis, Mexicana 13:61–65. Pontificia Univ. Cato´lica del Ecuador Facultad de TOFT, C. A. 1980. Feeding ecology of thirteen syntopic Ciencias Exactas y Naturales. Quito, Ecuador. species of anurans in a seasonal tropical environ- MONTORI, A. 1991. Alimentacioń de los adultos de ment. Oecologia 45:131–41. Euproctus asper (Duge´s, 1852) en la montan˜ a media VICTORIA,J.A.1999.Simulaciońmatema´tica del del Pirineo Catalań (Espan˜ a). Revista Espan˜ ola de sistema embalse de Ullum-Cuenca de agua sub- Herpetologıá 5:23–36. terrańea. Instituto Nacional del Agua y el Am- MORENO, C. E. 2001. Me´todos Para Medir La Biodi- biente Sede San Juan, San Juaan, Argentina. versidad. M&T-Manuales y Tesis SEA, Zaragoza, Spain. Accepted: 13 August 2008.

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