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Home , Abdon Batista, Chelidae, Phrynops, Phrynops williamsi, Uruguay River

Herpetology Notes, volume 11: 147-152 (2018) (published online on 10 February 2018)

New records, threats and conservation of williamsi (Testudines: ) in Southern

Tobias S. Kunz1,2, Ivo R. Ghizoni-Jr.1, Jorge J. Cherem1, Raissa F. Bressan1,2,*, Simone B. Leonardi2 and Juliana C. Zanotelli2

Abstract. We present new records of in southern Brazil and field observations that point to at least three threats to the in the Upper Basin. Our report provides for the first time direct observation of death and injuries as a consequence of falls from dams and walls of hydroelectric plants shortly after the reservoir formation, apparently as an attempt to abandon the artificial lakes; it also corroborates the species’ dependence on lotic environments, justifying the increasing concern with its conservation in southern Brazil.

Keywords: Geographic distribution, freshwater , hydroelectric dams, environmental licensing, Uruguay River

Introduction quality. This is mainly due to the sequential formation of hydroelectric dams in the Iguaçu and Uruguay river Phrynops williamsi Rhodin and Mittermeier, 1983 basins, respectively; because it has disappeared from is a poorly known freshwater turtle that inhabits free areas of these basins which were flooded after the flowing with rocky bottoms in southern Brazil, formation of hydroelectric reservoirs, apparently due Uruguay, north-eastern and south-eastern to the transformation of a lotic to a lentic environment. (Turtle Working Group, 2014). As a contribution to the knowledge of distribution and Even though it has not been globally assessed for conservation status of P. williamsi, we present new the IUCN Red List, P. williamsi has been assessed as records and field observations of the species in southern Vulnerable in Argentina (Prado et al., 2012), Paraguay Brazil. (Motte et al., 2009) and in the Brazilian states of Paraná (Bérnils et al. 2004) and (CONSEMA, Materials and Methods 2011). It was recently classified as Near Threatened in Uruguay (Carreira and Maneyro, 2015) and in the We compiled literature records for P. williamsi in Brazilian state of (FZB, 2014). In the State of Santa Catarina and field records obtained Brazil, on a national scale, the species was considered between 2005 and 2012, most of them during as Data Deficient (ICMBio, 2014). environmental studies and faunal monitoring for the In southern Brazil, its categorization as a vulnerable implementation of hydroelectric power plants located species in Paraná and Santa Catarina is based on in the Upper Uruguay River Basin (UURB), southern inferred reduction in population size due to declines Brazilian plateau, and records opportunistically obtained in area of occupancy, extent of occurrence and habitat at the Tubarão River Basin, southern coastal plain of Santa Catarina. Most of the records were obtained by visual searches from river margins or in boats. A small net of 10 m long and 1.8 m high composed by one mesh of 5 cm between 1 Caipora Cooperativa para a Conservação da Natureza, 88040- knots was used on only one occasion, during the 400, Florianópolis, Santa Catarina, Brazil 2 Laboratório de Herpetologia, Departamento de Zoologia, environmental study for the Garibaldi Power Plant, on Instituto de Biociências, Universidade Federal do Rio Grande the Canoas River, on January 2008. ������������������� do Sul, 91540-000, Porto Alegre, Rio Grande do Sul, Brazil were deposited in the herpetological collections of the * Corresponding author. E-mail: [email protected] Universidade Federal do Rio Grande do Sul, Porto 148 Tobias S. Kunz et al.

Figure 1. Records of Phrynops williamsi in the State of Santa Catarina (SC) and on the border of the State of Paraná (PR, North) and Rio Grande do Sul (RS, South), Southern Brazil. White circles represent literature records (Rhodin and Mittermeier, 1983; Cielusinsky et al., 2008; Kunz, 2012; Spier et al., 2014); black circles represent new records. Numbers correspond to localities described in Table 1.

Alegre (UFRGS), Universidade Federal de Santa Chapecó River in the municipality of Catarina, Florianópolis (CHUFSC), and Universidade (point 3). Three of these eggs presented the following Regional de Blumenau, Blumenau (FURB). measurements: 30.4 x 26.6 mm, 30.2 x 26.4 mm and

Results We obtained 10 new distribution records of P. williamsi for the State of Santa Catarina, two of them located at Table 1. Summary of the new records of Phrynops williamsi the border with the State of Rio Grande do Sul (Fig. 1; in southern Brazil, states of Santa Catarina (SC) and Rio Table 1). Of those, nine are for the UURB and one is Grande do Sul (RS). Locality numbers correspond to those in for the Tubarão River basin (point 13 of the map). We 1 FigureTable 1. 1.Summary of the new records of Phrynops williamsi in southern Brazil, states of Santa Catarina (SC) 2 and Rio Grande do Sul (RS). Locality numbers correspond to those in also obtained new records for three localities (points 2, 3 4 6-7) presented in Kunz (2012). Most of the records were River/Locality Altitude (m) Coordinates Chapecó River obtained by sightings of individuals basking on rocks 1. (SC) 1000 26.7130°S, 51.9069°W exposed in the middle of the river, near river . 2. Ipuaçu/São Domingos (SC) 470 26.6558°S, 52.5555°W All sightings were on lotic environments, previously 3. Coronel Freitas (SC) 340 26.8708°S, 52.7258°W Uruguay River to the damming, or in remaining lotic stretches up or 4. São Carlos (SC)/Alpestre (RS) 230 27.1466°S, 53.0463°W downstream the artificial lakes. One juvenile (CHUFSC 5. Chapecó (SC)/Erval Grande (RS) 245 27.2472°S, 52.5877°W 946) was caught by net at point 12 (now, the lake of the Irani River 6. Xanxerê/ (SC) 495 26.9527°S, 52.3372°W Garibaldi dam) and one adult individual with fractured 7. / (SC) 330 27.0555°S, 52.4711°W carapace (Fig. 2F) was caught in fishing net in front 8. /Chapecó (SC) 285 27.1830°S, 52.5244°W of (downstream) the Plano Alto dam (point 6) by the Peixe River 9. Tangará (SC) 590 27.1050°S, 51.2802°W ichthyologist of the faunal monitoring team. Two dead Marombas River individuals caught in nets (CHUFSC 1166, 1239; not 10. Frei Rogério/ (SC) 815 27.1827°S, 50.6702°W sexed) were obtained from local fisherman at point 5 Canoas River 11. Vargem/São José do Cerrito (SC) 715 27.4958°S, 50.8038°W (now, the lake of Foz do Chapecó dam). Also, a female 12. Cerro Negro/Abdon Batista (SC) 657 27.6302°S, 50.9741°W with nine eggs (Fig. 2A) was found hit by a vehicle Pequeno River on an unpaved road on December 12th, 2008, near the 13. Grão Pará (SC) 80 28.2180°S, 49.1950°W

 1 New records, threats and conservation of Phrynops williamsi in Brazil 149

Figure 2. Phrynops williamsi in the Upper Uruguay River basin. (A) Gravid female run-over at point 3 (see Figure 1, Table 1); (B) Adult male found headless in a fishing ranch near point 3; (C) Adult female dead after falling from a cliff at the Foz do Chapecó dam (point 4); (D-E) Specimens with fractured carapaces (indicated by arrows) observed in front of the Arvoredo dam (point 7); (F) Specimen with fractured carapace captured in front of the Plano Alto dam (point 6), Irani River.

28.5 x 26.4 mm. The record at Passos Maia dam (point Discussion 1) is the highest altitude recorded for the species (1000 Despite being frequently observed on river rapids - m a.s.l.). where on one occasion it was possible to count more than 30 individuals at the same time basking on rocks 150 Tobias S. Kunz et al.

(points 9 and 12) - observations made during faunal main food item of this species in the Iguaçu River basin monitoring and faunal rescue during the filling of (Cielusinsky et al., 2008), as these crustaceans are also the reservoirs suggest that individuals tend to move associated to rivers and streams of increased water flow downstream after the reservoir is completely full, (Noro and Buckup, 2003). apparently avoiding the new lentic environment The UURB is considered a Freshwater Ecoregion and eventually fall from the dam or its lateral walls, of the World (Abell et al., 2008) and, together with severely injuring their carapaces, sometimes fatally. the Parana and Paraguay rivers, it forms the La Plata This behaviour was reported by employees of the River basin, which is considered one of the ten most Arvoredo dam (point 7), where we observed individuals endangered river basins in the world, with the second with carapace injuries just in front of (downstream) largest number of hydroelectric dams planned (Wong et the dam (Fig. 2D-E). At the Foz do Chapecó dam, al., 2007). The Uruguay River is sequentially dammed after the reservoir filled, entered the water along the Santa Catarina - Rio Grande do Sul border catchment tunnel and emerged at the standpipe, where by the Machadinho, Itá and Foz do Chapecó dams (the there is a small reservoir (point 4). From this point last one alone impounded more than 100 km of the they followed a rock wall about five meters high next river). There are two large dams just upstream of the to the road that accesses the powerhouse; employees of the Canoas and Pelotas rivers (Campos reported that several individuals fell from this site. At Novos and Barra Grande dams, respectively), the main least two individuals died after falling (adult female, of the Uruguay River. Also, there are two FURB 11746, Fig. 2C and adult male, UFRGS 6551). other large dams downstream from Foz do Chapecó dam In fauna rescues during the filling of reservoirs, it was currently in process of environmental licensing, and at possible to get very near (Foz do Chapecó dam) and least two others are planned for the binational border of even collect specimens of P. williamsi with dip nets - Rio Grande do Sul (Brazil) - Misiones (Argentina). The two juveniles caught at Arvoredo (CHUFSC 1270) and number of planned dams on tributaries of the Uruguay Quebra Queixo dams (point 2; released downstream). River, only in the State of Santa Catarina, exceeds two These observations indicate that this species can become hundred according to the Brazilian Agency of Electric disoriented on these occasions, because normally Energy (ANEEL, 2014). individuals quickly submerge with the presence and Despite the major habitat loss caused by these artificial disturbance of people even a hundred meters away. flooding, only a few studies have documented the direct The bycatch of P. williamsi in fishing nets seems to be effect of the inundation of reservoirs for hydroelectric common according to reports from fishermen, who also power plants on wildlife (see Agostinho et al., 2008; reported the capture of turtles by hook. On December Mendonça et al,. 2009; Alho, 2011; Andriolo et al., 15th, 2008, an adult male was found dead, headless (Fig. 2013; Benchimol and Peres, 2015; Lima et al., 2015; 2B), in front of a house apparently used by fishermen, Sá-Oliveira et al., 2015). However, long-term studies near the Chapecó River, municipality of Quilombo (e.g. Mendonça et al., 2009; Benchimol and Peres, 2015; (near point 3). Cutting the neck to retrieve the hook Lima et al., 2015) have demonstrated severe impacts on seems to be a common practice reported by fishermen vertebrate diversity driven by large hydroelectric dams who accidentally catch freshwater turtles in fishing lines and questioned if hydropower is a low-impact energy in southern Brazil. source in the Neotropics. These studies highlighted that Our observations point to at least three threats to the the consequences of large dams on the biodiversity have conservation of P. williamsi in the UURB: bycatch been severely overlooked (Finer and Jenkins, 2012; in fishing nets and hooks, females hit by cars during Benchimol and Peres, 2015). the reproductive period, and death and injuries of Although P. williamsi still frequent observed in individuals as a consequence of falls from the walls of lotic environments of that river basin, it has suffered dams, probably as a result of the attempt to abandon an enormous habitat loss in southern Brazil due to recently formed reservoirs (lentic environment). proliferation of hydroelectric power plants. In this Among these threats, the latter seems more worrying, context, studies about the biology of P. williamsi, as it corroborates the dependence of this species to the especially regarding aspects related to its home range, lotic environment. Further evidence of the association reproduction and diet, are urgently required in to of P. williamsi with lotic environments was provided by properly measure how much impact the formation of the presence of crustaceans of the Aegla as the sequential dams brings to this species. New records, threats and conservation of Phrynops williamsi in Brazil 151

Acknowledgments. We would like to thank Bernd Marterer dá outras providências. ���������������������������������������� (in memoriam) for the photo and information of the individual Santa Catarina. recorded at the Plano Alto dam; Luís O. M. Giasson provided Finer, M., Jenkins, C.N. (2012): Proliferation of hydroelectric dams the photo of the individual deposited at FURB. We also thank in the Andean Amazon and implications for Andes-Amazon the companies ETS – Energia, Transporte e Saneamento and connectivity. �������� 7: e35126. Maurique Consultoria Ambiental for providing logistical support FZB (2014): Avaliação do Estado de Conservação de Espécies during the fieldwork. Permits were provided by the Brazilian Fauna - RS. ����������������������������������������������������� environmental agency (IBAMA; permits numbers 112/07, 113/07, modulo=1&id_uf=23&ano=2012. ������������������������ 013/2010 and 055/2010). ICMBio (2014): Lista de Espécies Quase Ameaçadas e com Dados Insuficientes. �������������������������������������� References portal/biodiversidade/fauna-brasileira/lista-de-especies-dados- insuficientes.html. Accessed on 7 July 2015. Abell, R., Thieme, M.L., Revenga, C., Bryer, M., Kottelat, M., Kunz, T.S (2012): Répteis. In: Fisiografia, Flora e Fauna do Rio Bogutskaya, N., Coad, B., Mandrak, N., Balderas, S.C., Irani, p. 103-116. ������������������������������������������������ Bussing, W., Stiassny, M.L.J., Skelton, P., Allen, G.R., Unmack, Brazil, ETS. P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Lima, J.R., Galatti, U., Lima, C.J., Fáveri, S.B., Vasconcelos, Higgins, J.V., Heibel, T.J., Wikramanayake, E., Olson, D., H.L., Neckel-Oliveira, S. (2015): Amphibians on Amazonian López, H.L., Reis, R.E., Lundberg, J.G., Pérez, M.H.S., Petry, land-bridge islands are affected more by area than isolation. P. 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Appendix. Collected specimens of Phrynops williamsi.

CHUFSC 946 (juvenile, 16 January 2008): Canoas River, between municipalities of Cerro Negro and Abdon Batista, State of Santa Catarina, 27.6302°S, 50.9741°W; CHUFSC 1166 (adult, sex not determined, October 2008) and CHUFSC 1239 (adult, sex not determined, March 2010): Uruguay River, between municipalities of Chapecó, state of Santa Catarina, and Erval Grande, State of Rio Grande do Sul, 27.2472°S, 52.5877°W); CHUFSC 1270 (juvenile, 10 February 2010): Irani River, between municipalities of Xaxim and Arvoredo, State of Santa Catarina, 27.0555°S, 52.4711°W; FURB 11746 (adult, female, 5 February 2011) and UFRGS 6551 (adult, male, 23 November 2012): UHE Foz do Chapecó, municipality of Alpestre, State of Rio Grande do Sul, 27.1466°S, 53.0463°W.

Accepted by Anamarija Zagar