First case of lordosis in a wild- caught European pond turtle (Emys orbicularis)

North-Western Journal of Zoology 2020, vol.16 (2) - Correspondence: Notes 242 Shine, R., Amiel, J., Munn, A.J., Stewart M., Vyssotski, A.L., Lesku, J.A. (2015): Is “cooling then freezing” a humane way to kill amphibians and reptiles? Biology Open 4: 760–763. Taylor, P.J., et al. (2009): Speciation mirrors geomorphology and palaeoclimatic history in African laminate-toothed rats (Muridae: Otomyini) of the Otomys denti and Otomys lacustris species complexes in the ‘Montane Circle’ of East Africa. Biological Journal of the Linnean Society 96: 913–941. Uetz, P., Hošek, J. (2019): The Reptile Database. Available from: <http://www.reptile-database.org> (accessed December 2019). 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 Hamzeh ORAIE1,2,* and Azar KHOSRAVANI3 1. Department of Zoology, Faculty of Science, Shahrekord University, Shahrekord, Iran. 2. Department of Biodiversity, Institute of Biotechnology, Shahrekord University, Shahrekord, Iran. 3. Iranian Plateau Herpetology Research Group (IPHRG), Faculty of Science, Razi University, 6714967346 Kermanshah, Iran. *Corresponding author, H. Oraie, E-mail: [email protected] First case of lordosis in a wildcaught European pond turtle (Emys orbicularis) Even though osteological abnormalities are very rare in wild reptiles (Telemaco et al. 2013, Löwenborg & Hagman 2017), they are more frequent in captivity as a consequence of a deficient care, especially related to nutrition and UV deficiencies (Mendyk 2008). In chelonians, in some cases, it is also related to soft shell and pyramidism (Museti et al. 2014). Kyphosis and lordosis are problems related to the vertebral column, namely kyphosis when the column is extruded and lordosis when the column is intruded. There are several cases of both anomalies described in lacertids (Garin-Barrio et al. 2011), skinks (Arrivillaga & Brown 2019) and sea turtles (Drenen 1990). Nevertheless, in freshwater turtles only kyphosis is relatively common (Saumure 2001, Trembath 2009, Moldowan et al. 2015), with few documented lordosis cases (Mitchell 2014; Selman 2019). In wild Emys orbicularis several deformities have been described such as microophtalmia (Escoriza 2012), axanthism (Cavalcante & Bruni 2018), pholydosis abnormalities as accessory scutes (Cordero et al. 2008) or accessory and absent scutes (Lada & Voldireva 2018). Here, we report the first case of lordosis in a European freshwater turtle (Emys orbicularis), being the first reported case of a lordotic wild turtle in Europe. The turtle was captured on the 22th July 2011 in “Río Areta”, which is a Special Area of Conservation (ES2200013), in Navarre (Spain), in a little cattle pond (42º42’N; -1º16’E), where the majority of turtles were juveniles (Table 1), including the lordotic turtle, showing a differential habitat selection among juveniles and adults (Ayres & Cordero 2007). It was a three-year-old turtle (CL = 46,6 mm, weight = 21 g) with algae encrusted on the carapace, and a concave deformity in the middle of the carapace (Fig.1). However, there was apparently no lack of mobility. The pond had a maximum depth of less than 1 meter, with Figure 1. Lordotic juvenile E.orbicularis with two normal shaped juveniles. Table 1. Measurements of the specimens captured in the pond where the lordotic turtle (in bold) was found. Sex was classified as M (male), F (female) or J (Juvenile with no external sexual characters). Weight was measured in grams and the carapace length (CL) in millimeters. ID Sex Weight (g) CL (mm) Neo10_04 J 12 38.49 Neo10_08 J 13 40.28 Neo10_02 J 13 40.38 Neo10_09 J 17 43.6 Neo10_05 J 17 45.16 Neo10_03 J 18 45.98 Neo09_04 J 21 46.63 Neo10_07 J 21 49.08 Neo10_06 J 22 49.49 Neo10_10 J 26 51.79 2454 J 72 73.28 2463 J 67 74.58 2450 F 141 92.26 2462 F 136 94.22 2446 F 152 97.76 2460 M 169 104.14 2465 M 207 111.7 2461 M 222 112.08 2457 F 260 112.76 2449 M 224 113.57 2455 M 234 118.79 2447 F 416 131.46 abundant water plants, macroinvertebrates and frogs. Neither fishes nor crayfishes were present in the pond, although they are present in the Areta River, where adult turtles commonly live. In addition, it is possible to consider the population and their individuals completely wild since the location was very far from cities, villages or touristic 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 carried to CRFS Ilundáin, where it was radiographed, and it was released again the following day in the pond where it was captured. In radiographs taken in dorso-ventral (Fig. 2A) and laterolateral (Fig. 2B) projection, the angle between the last cervical and first thoracic vertebrae as well as the top of lumbar vertebrae and the top of the sacrum vertebrae are clearly acute and not concavous. Neither fusion, demi-neralization North-Western Journal of Zoology 2020, vol.16 (2) - Correspondence: Notes 243 Figure 2. Radiographs taken in dorso-ventral (A) and latero-lateral (B) projection with 1cm white bar as scale, showing lordosis. nor infectious signs (local deformities or osteolysis) are observed in any affected vertebrae (Rotschild et al. 2013). However, Figure 2B shows that abnormal curvature affected not only the vertebral column but also the plastral bones. Ventral bones had a light lordotic curvature but with a less acute angle than the one observed in vertebral spine. Despite a common belief that lordosis could be a risk factor for back pain, behavioural evidences in this turtle revealed that there was no back pain symptoms during locomotion. Regarding the dermal scales, neither duplication or fusion, nor vertebral or costal scutes were observed. In reptiles, spinal malformations or spinal teratology can be due to incorrect conditions during the incubation of eggs, i.e. excessively low or high temperatures and low relative humidity; though notably, toxics and pollutants (e.g. insecticides) might also be responsible for malformations observed in wild reptiles (Bellairs 1981). Several hypotheses have been proposed to explain the origin of shell abnormalities in chelonians. Most of them are related to problems during embryonic or early juvenile development (Rothschild et al. 2013, Caracappa et al. 2016, Nagle et al. 2018, Zimm et al. 2018, Langer et al. 2020). There is evidence that polychlorinated biphenyls (PCBs), atrazine and glyphosate have a negative effect on bone development during incubation on freshwater turtles (Adams et al. 2016; Mendoçal et al. 2016). Additional studies have also shown that inbreeding of reptile 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 metabolic 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 deficiencies 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 organisms 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. References Adams, C.I.M., Baker, J.E., Kjellerup, B.V. 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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 NaturalesIUCA-Departamento de Geografía-Universidad de Zaragoza. C/Pedro Cerbuna, 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. Tafalla, Spain, E-mail: [email protected] 5. BASATI Veterinary N.G.O. Navarra region, Spain, E-mail: [email protected] 6. Catalonian Reptile and Amphibian Rehabilitation Center (CRARC) 08783, Masquefa, Spain. * Correspponding author, A. Valdeón, E-mail: [email protected] Unsuccessful predation attempt of Leptodactylus syphax (Anura: Leptodactylidae) on Acanthoscurria sp. (Araneae: Theraphosidae) Anurans are considered generalist and opportunistic predators, their gape and head size being the main constraints for the maximum prey size they can seize and ingest (Duellman & Trueb 1994, Ceron et al. 2018, Marques-Pinto et al. 2019). Frogs are important elements in the complex energy networks at tropical regions, since they feed on a wide variety of food items, such as insects and arthropods, and are preyed upon by a variety of animals such as snakes and small and medium mammals (Marques-Pinto et al. 2019, Zipkin et al. 2020). Spiders are commonly eaten by anurans (Solé et al. 2005, Sugai et al. 2012, Camera et al. 2014), mainly because they co-occur in environments used by frogs (Schalk & Sezano 2014). Conversely, spiders of the families Psauridae, Ctenidae, and Theraphosidae often feed on amphibians (Menin et al. 2005, Meneses et al. 2020). However, predation events of frogs consuming tarantulas are rare in nature, since these generally large spiders present a potential danger to their predators by wounding them with their setae and envenomating them using the chelicerae (Rosa et al. 2012, Bertani & Guadanucci 2013, Bogan & Eppehimer 2017, ValenciaValdez et al. 2019). Here we present a predation attempt on an Acanthoscurria sp. (Theraphosidae) by a Leptodactylus syphax Bokermann 1969. The event was observed on October 15, 2018, during night fieldwork of a remnant of native vegetation, near the Roncador Ecological Station, Brasília, Distrito Federal, Brazil (15°56'S, 47°48 'W, 1095 m a.s.l.). The frog was in an open rocky area (sensu Ribeiro & Walter 2008), holding the spider in its mouth when we located them. One of the spider's chelicera was penetrating the lower lip of the frog (Fig. 1). After 5 min the frog released the spider, but it was already dead. The frog left the area, not showing any obvious sign of distress. The observation was during the rainy season of the Cerrado, at a time that the males of both species are in their reproductive periods and actively searching for females (Silva & Giaretta 2009, Mota 2014), which could increase the chance of the two species encountering. Figure 1. An adult male Leptodactylus syphax attempting predation on an adult male Acanthoscurria sp. Note that at least one of the spider’s chelicerae is perforating the frog’s upper lip. Leptodactylus frogs use the “sit and wait” foraging strategy (Sugai et al. 2012, Ganci et al. 2018, Solé et al. 2019) that is typical for species with a generalist diet, largely based on invertebrates such as Blattaria, Coleoptera, Diptera, Hemiptera, Hymenoptera, Orthoptera, and Araneae (including Theraphosidae spiders; see Solé et al. 2005, Sugai et al. 2012, Teles et al. 2018). Leptodactylus syphax is a mid-sized frog belonging to the L. fuscus group (Sá et al. 2014), widely distributed 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 rocky outcrops, using rock cavities and termite burrows close to creeks as retreat sites (Heyer et al. 2010). Acanthoscurria is a Theraphosid genus of large Mygalomorph 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 setae on the retrolateral face of the palpal trochanter and by the presence of one tibial apophysis on the male’s leg I (Pérez-Miles et al. 1996). Seven species were recorded for the