First Case of Lordosis in a Wild- Caught European Pond Turtle (Emys

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

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Key words: Apathya yassujica, Intraspecific variability, Iran, mtDNA Cytb.

Article No: e207502 Received: 10. May 2020 / Accepted: 31. July 2020 Available online: 03. August 2020 / Printed: December 2020

Figure 1. Lordotic juvenile E.orbicularis with two normal shaped ju- Hamzeh ORAIE1,2,* and Azar KHOSRAVANI3 veniles.

1. Department of Zoology, Faculty of Science, Shahrekord University, Shahrekord, Iran. Table 1. Measurements of the specimens captured in the pond where 2. Department of Biodiversity, Institute of Biotechnology, Shahrekord Universi- the lordotic turtle (in bold) was found. Sex was classified as M ty, Shahrekord, Iran. (male), F (female) or J (Juvenile with no external sexual characters). 3. Iranian Plateau Herpetology Research Group (IPHRG), Faculty of Science, Weight was measured in grams and the carapace length (CL) in mil- Razi University, 6714967346 Kermanshah, Iran. limeters. *Corresponding author, H. Oraie, E-mail: [email protected] ID Sex Weight (g) CL (mm) Neo10_04 J 12 38.49 Neo10_08 J 13 40.28 First case of lordosis in a wild- caught Europe- Neo10_02 J 13 40.38 an pond turtle (Emys orbicularis) Neo10_09 J 17 43.6 Neo10_05 J 17 45.16 Even though osteological abnormalities are very rare in wild Neo10_03 J 18 45.98 reptiles (Telemaco et al. 2013, Löwenborg & Hagman 2017), Neo09_04 J 21 46.63 Neo10_07 J 21 49.08 they are more frequent in captivity as a consequence of a de- Neo10_06 J 22 49.49 ficient care, especially related to nutrition and UV deficien- Neo10_10 J 26 51.79 cies (Mendyk 2008). In chelonians, in some cases, it is also re- 2454 J 72 73.28 lated to soft shell and pyramidism (Museti et al. 2014). 2463 J 67 74.58 Kyphosis and lordosis are problems related to the verte- 2450 F 141 92.26 bral column, namely kyphosis when the column is extruded 2462 F 136 94.22 and lordosis when the column is intruded. There are several 2446 F 152 97.76 cases of both anomalies described in lacertids (Garin-Barrio 2460 M 169 104.14 et al. 2011), skinks (Arrivillaga & Brown 2019) and sea turtles 2465 M 207 111.7 (Drenen 1990). Nevertheless, in freshwater turtles only ky- 2461 M 222 112.08 phosis is relatively common (Saumure 2001, Trembath 2009, 2457 F 260 112.76 Moldowan et al. 2015), with few documented lordosis cases 2449 M 224 113.57 (Mitchell 2014; Selman 2019). 2455 M 234 118.79 In wild Emys orbicularis several deformities have been 2447 F 416 131.46 described such as microophtalmia (Escoriza 2012), axanthism (Cavalcante & Bruni 2018), pholydosis abnormalities as accessory scutes (Cordero et al. 2008) or accessory and ab- abundant water plants, macroinvertebrates and frogs. Neither fishes nor crayfishes were present in the pond, although they are present in sent scutes (Lada & Voldireva 2018). Here, we report the first the Areta River, where adult turtles commonly live. In addition, it is case of lordosis in a European freshwater turtle (Emys orbicu- possible to consider the population and their individuals completely laris), being the first reported case of a lordotic wild turtle in wild since the location was very far from cities, villages or touristic Europe. or recreational areas. Hence, it is very improbable that the animal could be maintained in captivity and released later in the wild. The turtle was captured on the 22th July 2011 in “Río Areta”, which The turtle was carried to CRFS Ilundáin, where it was radi- is a Special Area of Conservation (ES2200013), in Navarre (Spain), in ographed, and it was released again the following day in the pond a little cattle pond (42º42’N; -1º16’E), where the majority of turtles where it was captured. were juveniles (Table 1), including the lordotic turtle, showing a dif- ferential habitat selection among juveniles and adults (Ayres & In radiographs taken in dorso-ventral (Fig. 2A) and latero- Cordero 2007). It was a three-year-old turtle (CL = 46,6 mm, weight = lateral (Fig. 2B) projection, the angle between the last cervi- 21 g) with algae encrusted on the carapace, and a concave deformity in the middle of the carapace (Fig.1). However, there was apparently cal and first thoracic vertebrae as well as the top of lumbar no lack of mobility. vertebrae and the top of the sacrum vertebrae are clearly The pond had a maximum depth of less than 1 meter, with acute and not concavous. Neither fusion, demi-neralization North-Western Journal of Zoology 2020, vol.16 (2) - Correspondence: Notes 243

tile populations with low genetic diversity can cause malformations (Madsen et al. 1992; Olsson et al. 1996). In captive turtles, spinal malformations can also be caused by metabol- ic bone diseases (Frye 1991, Museti et al. 2014). In turtles, the thoracic and lumbar vertebrae cannot move in the join due to the fact that they merge forming aconvex column in the early stages of development (Pritchard 2008). In our case, the shell concavity and the absence of upright posture could have been developed since the first development stages of the turtle. Mineral deficien- cies were discarded by radiographic analyses, and the turtle seemed to have grown normally as well as the other turtles found in the pond, so that nutritional problems should not be the cause of the lordosis. Environmental pollutants are also a highly unlikely cause, as indicated by the absence of other affected animals such as turtles or other aquatic organ- isms around the area. As there was no shield fusion, the cause of the abnormality could be congenital.

Acknowledgements. European pond turtles were captured under licence of the Navarre Regional Government Number 581/2011. The CRFS Ilundáin, depending on the Government of Navarre and managed by the public enterprise ‘Gestión Ambiental de Navarra’,

assumed the costs of the radiographs.

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development of Podocnemis expansa (Testudines, Podocnemididae). Frogs 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 arthropods, and are Moldowan, P.D., Keevil, M.G., Kooper, N., Brooks, R.J., Litzgus, J.D. (2015): preyed upon by a variety of animals 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 Spiders 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 amphibians (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 tarantulas 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 Leptodactylus 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, Brazil (15°56'S, 47°48 'W, 1095 m a.s.l.). The frog 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 spider 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

Figure 1. An adult male Leptodactylus syphax attempting predation on Aitor VALDEÓN1,2,*, César AYRES3, Virginia RADA4, an adult male Acanthoscurria sp. Note that at least one of the spi- 5 6 Alfonso BAÑERES and Albert MARTÍNEZ-SILVESTRE der’s chelicerae is perforating the frog’s upper lip.

1. Grupo de investigación Clima, Agua, Cambio Global y Sistemas Naturales- IUCA-Departamento de Geografía-Universidad de Zaragoza. C/Pedro Cer- Leptodactylus frogs use the “sit and wait” foraging strate- buna, 12. 50009 Zaragoza. Spain. 2. Dpto. Herpetología. Sociedad de Ciencias Aranzadi. Zorroagagaina 11. 20014 gy (Sugai et al. 2012, Ganci et al. 2018, Solé et al. 2019) that is Donostia-San Sebastián. Spain typical for species with a generalist diet, largely based on in- 3. AHE-Galicia. Barcelona, 86, 6C. 36211, Vigo (Pontevedra). Spain. vertebrates such as Blattaria, Coleoptera, Diptera, Hemip- 4. Tafalla, Spain, E-mail: [email protected] tera, Hymenoptera, Orthoptera, and Araneae (including 5. BASATI Veterinary N.G.O. Navarra region, Spain, E-mail: [email protected] 6. Catalonian Reptile and Amphibian Rehabilitation Center (CRARC) 08783, Theraphosidae spiders; see Solé et al. 2005, Sugai et al. 2012, Masquefa, Spain. Teles et al. 2018). Leptodactylus syphax is a mid-sized frog be- * Correspponding author, A. Valdeón, E-mail: [email protected] longing to the L. fuscus group (Sá et al. 2014), widely distrib-

uted in Brazil (especially in the Cerrado, Caatinga and Chaco

biomes), with records in Bolivia and Paraguay (Andrade et al. 2011). It is commonly associated with open areas with Unsuccessful predation attempt of rocky outcrops, using rock cavities and termite burrows Leptodactylus syphax (Anura: close to creeks as retreat sites (Heyer et al. 2010). Leptodactylidae) on Acanthoscurria sp. Acanthoscurria is a Theraphosid genus of large Mygalo- (Araneae: Theraphosidae) morph spiders, with species in the Cerrado reaching up to 80 mm in body length (cephalothorax + abdomen; Motta 2014).

These spiders can be identified by their distinct stridulatory Anurans are considered generalist and opportunistic preda- setae on the retrolateral face of the palpal trochanter and by tors, their gape and head size being the main constraints for the presence of one tibial apophysis on the male’s leg I (Pé- the maximum prey size they can seize and ingest (Duellman rez-Miles et al. 1996). Seven species were recorded for the & Trueb 1994, Ceron et al. 2018, Marques-Pinto et al. 2019).