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244 North-Western Journal of Zoology 2020, vol.16 (2) - Correspondence: Notes

development of Podocnemis expansa (Testudines, Podocnemididae). are important elements in the complex energy net- International Journal of Pure and Applied Zoology 4: 142-148. works at tropical regions, since they feed on a wide variety Mitchell, J.C. (2014): Chrysemys picta picta (Eastern Painted Turtle). Lordosis. Herpetological Review 45(2): 311. of food items, such as insects and , and are Moldowan, P.D., Keevil, M.G., Kooper, N., Brooks, R.J., Litzgus, J.D. (2015): preyed upon by a variety of such as snakes and Growth, sexual maturity, and reproduction of a female Midland Painted small and medium mammals (Marques-Pinto et al. 2019, Turtle (Chrysemys picta marginata) afflicted with kyphosis. Chelonian Conservation and Biology 14(2): 157-160. Zipkin et al. 2020). Museti, M.R., Aoki, M., Pinheiro, S.R. (2014): Reabilitação de jabuti (Chelonoidis are commonly eaten by anurans (Solé et al. 2005, carbonaria) com problema de casco: relato de caso. Scientia Vitae. Revista Sugai et al. 2012, Camera et al. 2014), mainly because they Electronica Academica 1: 91-96. Nagle, R.D., Rowe, C.L., Grant, C.J., Sebastian, E.R., Martin, B.E. (2018): co-occur in environments used by frogs (Schalk & Sezano Abnormal Shell Shapes in Northern Map Turtles of the Juniata River, 2014). Conversely, spiders of the families Psauridae, Cte- Pennsylvania, USA. Journal of Herpetology 52(1): 59-66. nidae, and Theraphosidae often feed on (Menin Olsson, M., Gullberg, A., Tegelström, H. (1996): Malformed offspring, sibling matings, and selection against inbreeding in the sand lizard (Lacerta agilis). et al. 2005, Meneses et al. 2020). However, predation events Journal of Evolutionary Biology 9: 229-242. of frogs consuming are rare in nature, since these Pritchard, P.C.H. (2008): Evolution and structure of the turtle shell. 45-83. In: generally large spiders present a potential danger to their Wyneken, J., Godfrey, M.H., Bels, V. (eds.), Biology of turtles. Boca Raton. predators by wounding them with their setae and enven- CRC Press. Rothschild, B.M., Schultze, H.P., Pellegrini, R. (2013): Osseous and other hard omating them using the chelicerae (Rosa et al. 2012, Bertani tissue pathologies in turtles and abnormalities of miner deposition. In: & Guadanucci 2013, Bogan & Eppehimer 2017, Valencia- Brinkman, R.B., Holroyd, P.A., and Gardner, J.D. (Eds.). Morphology and Valdez et al. 2019). Evolution of Turtles. New York: Springer, pp. 501–534. Selman, W. (2019): Malaclemys terrapin (Diamond-backed Terrapin). Kyphosis Here we present a predation attempt on an Acantho- and Lordosis. Herpetological Review 50(4): 774-775. scurria sp. (Theraphosidae) by a syphax Boker- Saumure, R.A. (2001): Kyphosis in a musk turtle (Sternotherus odoratus) from mann 1969. The event was observed on October 15, 2018, Ontario, Canada. Chelonian Conservation and Biology 4(1): 159. Telemeco, R.S., Warner, D.A., Reida, M.K., Janzen, F.J. (2013): Extreme during night fieldwork of a remnant of native vegetation, developmental temperatures result in morphological abnormalities in near the Roncador Ecological Station, Brasília, Distrito Fed- painted turtles (Chrysemys picta): a climate change perspective. Integrative eral, (15°56'S, 47°48 'W, 1095 m a.s.l.). The was in Zoology 8(2): 197-208. Trembath, D.F. (2009): Kyphosis of Emydura macquarii krefftii (Testudines: an open rocky area (sensu Ribeiro & Walter 2008), holding Chelidae) from Townsville, Queensland, Australia. Chelonian Conservation the in its mouth when we located them. One of the and Biology 8(1): 94-95. spider's chelicera was penetrating the lower lip of the frog Zimm, R., Bentley, B.P., Wyneken, J., Moustakas-Verho, J.E. (2017): (Fig. 1). After 5 min the frog released the spider, but it was Environmental Causation of Turtle Scute Anomalies in ovo and in silico. Integrative and Comparative Biology 57(6): 1303-1311. already dead. The frog left the area, not showing any obvi- ous sign of distress. The observation was during the rainy Key words: osteological abnormalities, Emydidae, Spain, herpetology, season of the Cerrado, at a time that the males of both spe- teratology. cies are in their reproductive periods and actively searching

for females (Silva & Giaretta 2009, Mota 2014), which could Article No: e207503 Received: 23. June 2020 / Accepted: 19. August 2020 increase the chance of the two species encountering. Available online: 23. August 2020 / Printed: December 2020

Aitor VALDEÓN1,2,*, César AYRES3, Virginia RADA4, Alfonso BAÑERES5 and Albert MARTÍNEZ-SILVESTRE6

1. Grupo de investigación Clima, Agua, Cambio Global y Sistemas Naturales- IUCA-Departamento de Geografía-Universidad de Zaragoza. C/Pedro Cer- buna, 12. 50009 Zaragoza. Spain. 2. Dpto. Herpetología. Sociedad de Ciencias Aranzadi. Zorroagagaina 11. 20014 Donostia-San Sebastián. Spain 3. AHE-Galicia. Barcelona, 86, 6C. 36211, Vigo (Pontevedra). Spain. 4. Zaragosa, Spain, E-mail: [email protected] 5. BASATI Veterinary N.G.O. Zaragosa, Spain, E-mail: [email protected] 6. Catalonian Reptile and Rehabilitation Center (CRARC) 08783, Masquefa, Spain. * Corresppnding author, A. Valdeón, E-mail: [email protected]

Figure 1. An adult male Leptodactylus syphax attempting predation on an adult male sp. Note that at least one of the spi- der’s chelicerae is perforating the frog’s upper lip. Unsuccessful predation attempt of Leptodactylus syphax (Anura: Leptodactylus frogs use the “sit and wait” foraging strate- ) on Acanthoscurria sp. gy (Sugai et al. 2012, Ganci et al. 2018, Solé et al. 2019) that is (Araneae: Theraphosidae) typical for species with a generalist diet, largely based on in- vertebrates such as Blattaria, Coleoptera, Diptera, Hemip- Anurans are considered generalist and opportunistic preda- tera, Hymenoptera, Orthoptera, and Araneae (including tors, their gape and head size being the main constraints for Theraphosidae spiders; see Solé et al. 2005, Sugai et al. 2012, the maximum prey size they can seize and ingest (Duellman Teles et al. 2018). Leptodactylus syphax is a mid-sized frog be- & Trueb 1994, Ceron et al. 2018, Marques-Pinto et al. 2019). longing to the L. fuscus group (Sá et al. 2014), widely distrib- North-Western Journal of Zoology 2020, vol.16 (2) - Correspondence: Notes 245 uted in Brazil (especially in the Cerrado, Caatinga and Chaco Camera, B., Krinski, D., Calvo, I. (2014): Diet of the Neotropical frog biomes), with records in and (Andrade et Leptodactylus mystaceus (Anura: Leptodactylidae). Herpetology Notes 7: 31- 36. al. 2011). It is commonly associated with open areas with Ceron, K., Moroti, M.T., Benício, R.A., Balboa, Z.P., Marçola, Y., Pereira, L.B., rocky outcrops, using rock cavities and termite burrows Santana, D.J. (2018): Diet and first report of batracophagy in Leptodactylus close to creeks as retreat sites (Heyer et al. 2010). podicipinus (Anura: Leptodactylidae). Neotropical Biodiversity 4: 70-74. Cooke, J.A., Roth, V.D., Miller, F.H. (1972): The urticating hairs of theraphosid Acanthoscurria is a Theraphosid of large Mygalo- spiders. American Museum Novitates 2498: 1-43. morph spiders, with species in the Cerrado reaching up to 80 Duellman, W.E., Trueb, L. (1994): Biology of Amphibians. 2nd Edition. The mm in body length (cephalothorax + abdomen; Motta 2014). Johns Hopkins University Press, Baltimore. Ganci, C.C., Silva, L.A., Pacheco, O., Nogueira, M.T., Santana, D. (2018): Diet These spiders can be identified by their distinct stridulatory and sexual dimorphism of Leptodactylus labyrinthicus (Anura, setae on the retrolateral face of the palpal trochanter and by Leptodactylidae) in a Cerrado area in Central Brazil. North-Western Journal the presence of one tibial apophysis on the male’s leg I (Pé- of Zoology 14: 250-254. Heyer, W.R., Heyer, W.W., Sá, R.O. (2010): Leptodactylus syphax. Catalogue of rez-Miles et al. 1996). Seven species were recorded for the American Amphibians and Reptiles 868: 1-9. Cerrado biome, four of which occur in the Distrito Federal Marques-Pinto T., Barreto-Lima, A.F., Brandão, R.A. (2019): Dietary resource area (A. gomesiana, A. natalensis, A. paulensis, and A. tarda; use by an assemblage of terrestrial frogs from the Brazilian Cerrado. North- Motta 2014). They can be found in a variety of microhabitats Western Journal of Zoology 15: 135-146. Menin, M., Rodrigues, D.J., Azevedo, C.S. (2005): Predation on amphibians by and utilize cover such as logs, under rocks, termite nests, spiders (Arachnida, Araneae) in the neotropical region. Phyllomedusa 4: 39- holes (Motta 2014). 47. Theraphosid spiders were rarely recorded as a diet item Meneses, ASO, Corrêa, BAAP, Fernandes, MDAR, Lopes, BEPC, Citeli, NK, Brandão, RA (2020): What size of Neotropical frogs from spiders prey on? for Leptodactylus or other frogs (Rosa et al. 2012). Tarantulas Biology 75: 1-16. are rarely predated as they present a series of defenses such Mourão, C.B.F., Oliveira, F.N., Carvalho, A.C., Arenas, C.J., Duque, H.M., as the presence of stinging hairs (urticating setae) along the Gonçalves, J.C., Macêdo, J.K.A., Galante, P., Schwartz, C.A., Mortari, M.R., Santos, M.F.M., Schwartz, E.F. (2013): Venomic and pharmacological activity body that are used against vertebrates, mainly mammals. of Acanthoscurria paulensis (Theraphosidae) spider venom. Toxicon 61: 129- (Cooke et al. 1972, Bertani & Guadanucci 2013). Currently, 138. five types of urticating setae are recognized (Types I–V) that Motta, P.C. (2014): Aracnídeos do Cerrado. 1st Edition. Technical Books Press, Brasília, Brazil. can be identified by their morphology, length, and adorn- Pérez-Miles, F., Lucas, S.M., Silva, P.I., Bertani, R. (1996): Systematic revision ments (Bertani & Guadanucci 2013). Acanthoscurria spp. have and cladistic analysis of (Araneae: Theraphosidae). type III setae, which are characterized by being the longest Mygalomorph 1: 33-68. (0.3–1.2 mm), with sharp points and some barbs laterally, Ribeiro, J.F., Walter, B.M.T. (2008): As principais fitofisionomias do bioma Cerrado. pp. 151-212. In: Sano, S.M., Almeida, S.P., Ribeiro, J.F. (eds.), which favor deeper penetration, causing serious irritations Cerrado: Ecologia e Flora. Embrapa Cerrados. (Cooke et al. 1972). In addition to the setae, the action of the Rosa, G.M., Bradfield, K., Fernández-Loras, A., Garcia, G., Tapley, B. (2012): venom of the genus Acanthoscurria proved to be effective in Two remarkable prey items for a chicken: Leptodactylus fallax Müller, 1926 predation upon the theraphosid spider femoralis Pocock, 1903 and vertebrates, causing cardiac problems in frogs during exper- the colubrid snake Liophis juliae (Cope, 1879). Tropical Zoology 25: 135-140. imental setups, but these effects still need to be tested in the Sá, R.O., Grant, T., Camargo, A., Heyer, W.R., Ponssa, M.L., Stanley, E. (2014): predatory context in the field (Mourão et al. 2013). Systematics of the neotropical genus Leptodactylus Fitzinger, 1826 (Anura: Leptodactylidae): phylogeny, the relevance of non–molecular evidence, and This is the first record of attempted predation of a taran- species accounts. South American Journal of Herpetology 9 (Special Issue 1): tula by an L. syphax and the second report for the genus Lep- S1-S128. todactylus in the Neotropical region. A similar observation Schalk, C., Sezano, M. (2014): Observations on the use of burrows by the anurans Leptodactylus bufonius (Leptodactylidae) and Rhinella major was reported from the neotropics, where a Leptodactylus (Bufonidae) in the Dry Chaco ecoregion of Bolivia. Acta Herpetologica 9: 99- fallax successfully preyed on a tarantula, Cyrtopholis femoralis, 102. which also has the type III setae (Rosa et al. 2012). This in- Silva, W.R., Giaretta, A.A. (2009): On the natural history of Leptodactylus syphax creases our knowledge of ecological interactions involving with comments on the evolution of reproductive features in the L. pentadactylus species group (Anura, Leptodactylidae). Journal of Natural two predators at a similar trophic level that caused the death History 43: 191-203. of at least one of them. We assume that the frog, if it sur- Solé, M., Beckmann, O., Pelz, B., Kwet, A., Engels, W. (2005): Stomach-flushing vived the encounter, probably will avoid further large-sized for diet analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests, southern Brazil. Studies on Neotropical Fauna and spiders as a potential prey (Bernal et al. 2007). Environment 40: 23-28. Solé, M., Dias, I.R., Rodrigues, E.A., Marciano-Jr, E., Branco, S.M., Roedder, D. Acknowledgments. We are grateful to the financial support (2019): Diet of Leptodactylus spixi (Anura: Leptodactylidae) from a cacao provided by CAPES and CNPQ, by the grant to N. K. C. (CAPES, plantation in southern Bahia, Brazil. North-Western Journal of Zoology 15: 62-66. process 88882.384453) and the grant to A. S. O. M (CNPQ, process Sugai, J.L.M.M., Terra, J.D.S., Ferreira, V.L. (2012): Diet of Leptodactylus fuscus 127236/2019-8). We thank two anonymous reviewers. (Amphibia: Anura: Leptodactylidae) in the Pantanal of Miranda river, Brazil. Biota Neotropica 12: 99-104. References Teles, D.A., Rodrigues, J.K., Teixeira, A.M., Araujo-Filho, J.A., Sousa, J.G.G., Andrade, E.B., Guimarães, R., Leite Jr, J.M.A., Leite, J.R.S. (2011): Amphibia, Ribeiro, S.C. (2018): Diet of Leptodactylus macrosternum (Miranda–Ribeiro Anura, Leptodactylidae, Leptodactylus syphax Bokermann, 1969: Distribution 1926) (Anura: Leptodactylidae) in the Caatinga domain, Northeastern Brazil, extension and geographic distribution map. Check List 7: 592-593. Neotropical Region. Herpetology Notes 11: 223-226. Bernal, X.E., Stanley Rand, A., Ryan, M.J. (2007): Sexual differences in the Valencia-Valdez, J.M., Cruz-Sáenz, D., Villarreal-Hernández, H., Hernández- behavioral response of túngara frogs, Physalaemus pustulosus, to cues Dávila, L.A., de Luna, M., Alcalá-Beltrán, L.Á., Lazcano, D. (2019): Notes on associated with increased predation risk. Ethology 113: 755-763. the Herpetofauna of Western Mexico 22: A new food item for the Mexican Bertani, R., Guadanucci, J.P.L. (2013): Morphology, evolution and usage of leaf frog, Agalychnis dacnicolor: The tarantula Bonnetina sp. (Mexican Blue urticating setae by tarantulas (Araneae: Theraphosidae). Zoologia 30: 403- Beauty). Bulletin of the Chicago Herpetological Society 54: 49-56. 418. Zipkin, E.F., DiRenzo, G.V., Ray, J.M., Rossman, S., Lips, K. R. (2020): Tropical Bogan, M.T., Eppehimer, D.E. (2017): Attempted predation of western desert snake diversity collapses after widespread amphibian loss. Science 367: 814- tarantula by sonoran desert toad. The Southwestern Naturalist 62: 146-148. 816.

246 North-Western Journal of Zoology 2020, vol.16 (2) - Correspondence: Notes

Key words: Anura, , ambush, tarantula, Cerrado, Brazil. eggs were incubated at room temperature (24-26°C) and the soil was moistened periodically (almost every day). Because of the unknown Article No: e207504 date/period of egg laying, we could not determine the exact incuba- Received: 25. March 2020 / Accepted: 07. September 2020 tion period, but after 10-14 days, all eggs had hatched successfully Available online: 13. September 2020 / Printed: December 2020 (Fig. 1A). After hatching, each individual was photographed and

measured on the next day. The snout-vent length (SVL) and the tail

length (TL) were taken with a plastic ruler, and the weight (W) was Bruno Alessandro Augusto Peña CORRÊA1,2,*, taken with an electronic weighting scale MXX-123 (Denver Instru- 2,3 Afonso Santiago de Oliveira MENESES , ment, NY, USA) with accuracy of 0.01 g. After the measurements, all Bruno Eduardo Pires de Camargos LOPES2, lizards were released in the nearest large meadow in the same dis- Mateus de Alencar Ramos FERNANDES2, trict. Nathalie Kaladinsky CITELI1,2 and Reuber Albuquerque BRANDÃO2 The number of eggs we found (seven) corresponds to the species’ clutch size mentioned in the literature – between 2 1. Institute of Biology, Department of Physiological Sciences, University of Bra- and 19 eggs (see Roitberg et al. 2015). sília, Laboratory of Comparative Anatomy of Vertebrates, Brasília, Distrito Federal, Brazil. All seven measured juveniles (Tab. 1, Fig. 1B) were with 2. University of Brasília, Department of Forest Engineering, Faculty of Technol- SVL of 30-31 mm and W of 0.41-0.56 g (Tab. 1). ogy, Laboratory of Fauna and Conservation Units, Brasília, Distrito Federal, The mean mass of the hatchlings was 0.49 g and the Brazil. mean SVL was 30.26 mm (see Tab. 1). Tzankov (2007) and 3. Laboratory of Herpetology, Department of Zoology, Museu Paraense Emílio Goeldi, Belém, Pará, Brazil. Stojanov et al. (2011) mentioned that the hatchlings of L. *Corresponding author, B.A.A.P. Corrêa, E-mail: [email protected] agilis for Bulgaria have a SVL of 30 mm and 27.2 mm. In both sources, the origin of that information is not stated, but most likely it refers to what is published for the species in other countries. The mass and SVL of the hatchlings for other Notes on some biometrical data on hatchlings of Lacerta agilis (L.) (Squamata: Lacertidae) in Western Bulgaria Figure 1. The juveniles of L. agilis in the present study. A – hatching of a juvenile, B – measuring a juvenile’s weight, C – the juveniles The Sand lizard Lacerta agilis Linnaeus, 1758 is one of the before releasing them back into the wild. three lizards from the genus Lacerta L. in Bulgaria. The sub- species L. a. chersonensis Andrzejowski, 1832 is sporadically Table 1. Measurements of the snout-vent length (SVL), weight (W) distributed in Western Bulgaria with single localities on the and tail length (TL), with mean and min-max values of the hatch- Northern Black Sea Coast and Strandzha Mts. (Stojanov et al. lings of L. agilis.

2011, Tzankov et al. 2014). Juvenile SVL (mm) TL (mm) Weight (g) There are many studies from different parts of the range 1 30 35.5 0.47 of the species, dealing with its reproductive biology and fe- 2 30 36.6 0.48 cundity (Jensen 1982, Olsson & Shine 1997a,b, in den Bosch 3 30.3 37 0.54 & Bout 1998, Amat et al. 2000, Roitberg et al. 2015), but to 4 30.5 38.5 0.56 our knowledge published data from the Balkans are lacking. 5 31 36 0.51 Furthermore, there are no papers concerning the life cycle of 6 30 36.3 0.41 the species in Bulgaria, just few on some ecological aspects 7 30 37.5 0.44 and microhabitat preferences (Grozdanov et al. 2014; Popova Mean 30.26 36.77 0.49 et al. 2020). Min-Max 30.00-31.00 35.50-38.50 0.41-0.56 Up to date, there are only few studies and observations on the reproduction of different lizard species in Bulgaria. countries vary from mean 0.59 g (from wild females), to 0.61 Mollov (2011) and Undjian (2000) present data on the egg g (from laboratory-raised animals) for Swedish populations size in Mediodactylus kotschyi (Steindachner, 1870), while of L. a. agilis L. (Olsson & Shine 1997a). Again, for L. a. agilis Garbov (1990) and Vergilov et al. (2018) provide information in den Bosch & Bout (1998) give the following mean values on the reproduction and eggs of Ablepharus kitaibelii (Bibron for the SVL and mass of the hatchlings: 24.6 mm and 0.70 g. & Bory de Saint-Vincent, 1833). The only data for Bulgaria For a Chinese population of the species, Li et al. (2011) give on hatchling size of a lizard species are those of Vergilov & the following mean values of SVL and mass depending on Natchev (2018) again, for A. kitaibelii. No data on the hatch- the different temperature of incubation – between 33.3 mm ling size or the life cycle of any other species from the coun- and 34.5 mm for SVL and between 0.76 g and 0.87 g for try have been published so far. themass. The mass of the hatchlings of our study is closer to In the current study, data on the snout-vent length, tail that of juveniles from wild females (Olsson & Shine 1997a), length and weight of newly hatched individuals of L. agilis probably because of the fact that most of the time the eggs in are presented. our study were incubated in natural conditions. To our knowledge, our data are the first for any lacertid species, In August 2014, seven eggs of L. agilis chersonensis were found in the where eggs were found in the wild, incubated, and the garden of a house in Benkovski district, Sofia, Bulgaria. The eggs hatchlings were subsequently measured. Some caution is were carefully removed from the garden (due to agricultural activi- needed, of course, when comparing the results of our study ties) and placed in soil in a plastic box with vol. app. 500 ml. The to those in other publications, because of the differences in