Herpetology Notes, volume 13: 1103-1106 (2020) (published online on 28 December 2020)

Haementeria sp. (Clitellata: Hirudinea) parasitising Phrynops geoffroanus (Testudines: Chelidae) in limnetic ecosystems of northeastern Brazil

Daniel Oliveira Santana1,2,*, Júlio César Victor Pereira3, Bruno Romão3, Erly de Lima Ferreira3, and Silvio Felipe Barbosa Lima2,3

Parasitism is a disharmonious symbiotic relationship We report here the observation of an adult P. between two species in which the parasite benefits at the geoffroanus close to an artificial pond at 07:00 PM expense of a host (Gibbons et al., 2000; Silva and Araújo, on 30 June 2019 in an urban area of the Municipality 2008; Pereira et al., 2018). Leeches are carnivorous or of Cajazeiras in the State of Paraíba, northeast Brazil hematophagous ectoparasites of various invertebrates (6.8822ºS, 38.5572ºW). The event occurred in the early and vertebrates (Bielecki et al., 2012). Leech species of evening, which is a period freshwater turtles occasionally the genus Haementeria occur throughout the Neotropical use to move between different water bodies (Rueda- region (Siddall and Borda, 2004; Christoffersen, 2007) Almonacid et al., 2007; Santana et al., 2016). The and aquatic species are often parasites of crocodilians specimen was captured manually and the presence of a and freshwater turtles (Sawyer and Kinard, 1980; Hirudinea was detected in the ventral region. The leech Sawyer, 1986). In chelonians, these parasites normally was narcotised using to method described by Klemm occupy soft body parts favourable to fixation, such as (1995), which consists of soaking in 10% ethanol to the pleural cavity of the arms and legs, neck, tail, and facilitate removal. The ectoparasite was removed with even the mouth (Herbst, 1994; Rodrigues and Silva, forceps, fixed in 4% formaldehyde, and preserved in 2015; Santana et al., 2019). 70% ethanol. The chelonian was then released into Phrynops geoffroanus is a medium-sized freshwater a nearby stream 500 m from the capture site. In the turtle (Rueda-Almonacid et al., 2007) with broad laboratory, the parasite was identified using characters geographic distribution in South America, occurring proposed for the genus by Oceguera-Figueroa (2012). A from the Colombian Amazon to southern Brazil and voucher specimen (COMAT_ANE 001) was deposited northern Argentina (Pritchard and Trebbau, 1984; Ernst in the Invertebrate Collection the Universidade Federal and Barbour, 1989). It is found in the main hydrographic de Campina Grande (UFCG/CFP). The parasite basins of the region and occurs in different aquatic belonged to the genus Haementeria (Hirudinea) (Fig. environments, such as rivers, streams, and lakes (Rueda- 1), characterised by one pair of eyespots, the presence Almonacid et al., 2007; Moura et al., 2015; Costa et al., of Lang’s organ, 11 longitudinal lines of tubercles; mid- 2018). This species is also commonly recorded in urban body somites primarily triannulate, [(a1) + (a2) + (a3)], environments (Souza and Abe, 2001; Martins et al., according to Oceguera-Figueroa (2012). It was found 2010). strongly affixed to the posterior ventral region of the chelonian, with jaws attached to the left anal plate of the carapace and the sucker affixed at the bottom of the left supracaudal anal plate of the plastron (Fig. 2). 1 Departamento de Ecologia, Universidade Federal de Sergipe, The parasite-host relationship of Hirudinea associated Cidade Universitária, São Cristóvão, Sergipe 49100-000, with testudines is poorly studied in limnetic ecosystems Brazil. of the Neotropical region (Brites and Rantin, 2004; 2 Departamento de Sistemática e Ecologia, Universidade Federal Santana et al., 2019). In a recent study, Santana et al. da Paraíba, Cidade Universitária, João Pessoa, Paraíba 58059- (2019) found individuals of the genus Haementeria 900, Brazil. 3 Centro de Formação de Professores, Universidade Federal de infesting P. geoffroanus in limnetic ecosystems in Campina Grande, Cajazeiras, Paraíba 58900-000, Brazil. the Caatinga and Atlantic Forest biomes of northeast * Corresponding author. E-mail: [email protected] Brazil. The authors identified and described Hirudinea 1104 Daniel Oliveira Santana et al.

Figure 1. Haementeria sp. in the Municipality of Cajazeiras, State of Paraíba, northeast Brazil. (A) Ventral view. (B) Dorsal view. (C) Ventral view of head region with pair of eyespots (detail). (D) Dorsal views (detail). Scale bars: 5 mm (A and B) and 2 mm (C and D). Photos by Silvio F.B. Lima.

Figure 2. Haementeria sp. parasitising Phrynops geoffroanus in the Municipality of Cajazeiras, State of Paraíba, northeast Brazil. (A)Ventral view of P. geoffroanus. (B and C) Dorsal view and left side views (detail) of Haementeria sp. on carapace and plastron of P. geoffroanus. Scale bar: 5 mm. Photos by Silvio F.B. Lima. Haementeria sp. parasitising Phrynops geoffroanus in northeastern Brazil 1105 infesting P. geoffroanus and Mesoclemmys tuberculata, Review of Fish Diseases 4: 389–425. demonstrating that these ectoparasites can be found Klemm, D.J. (1995): Identification Guide to the Freshwater Leeches on different parts of the chelonian body but are more (Annelida: Hirudinea) of Florida and Other Southern States, Tallahassee – Florida. Tallahassee Florida, USA, Department of frequent in hind limb cavities. In contrast, the present Environmental Protection. record demonstrates a host condition out of the water, Martins, F.I., Souza, F.L., Costa, H.T.M. (2010): Feeding Habits of which was not tested by Santana et al. (2019). The Phrynops geoffroanus (Chelidae) in an Urban River in Central specimen was not attached to soft body parts, but rather Brazil. Chelonian Conservation and Biology 9: 294–297. to the plastron. The fact that the host was recorded Moura, C., Moura, G., Chaves, L., Muniz, S., Vega, E.S., Júnior, outside the water may have affected the position of the V. (2015): Demography, sex ratio, and sexual dimorphism of Testudines in Araripe Bioregion, Ceará, Northeastern Brazil. leech and the low infestation intensity. North-Western Journal of Zoology 11: 204–212. The ‘‘desiccating leech’’ hypothesis support low Oceguera-Figueroa, A. (2012): Molecular phylogeny of the New infestation levels, as basking behaviour and movements World bloodfeeding leeches of the genus Haementeria and out of the water lead to the detachment of leeches due to reconsideration of the biannulate genus Oligobdella. Molecular desiccation. However, some leeches may be considerably Phylogenetics and Evolution 62: 508–514. more resistant to desiccation than is commonly assumed Pereira, A.M.A., Brito, S.V., Araujo Filho, J.A., Teixeira, A.A.M., (Vogt, 1979). Teles, D.A., Santana, D.O., et al. (2018): Diet and helminth parasites of freshwater turtles Mesoclemmys tuberculata, Little is known regarding the dynamics of parasites Phrynops geoffroanus (Pleurodira: Chelidae) and Kinosternon in natural populations of reptiles, especially freshwater scorpioides (Criptodyra: Kinosternidae) in a semiarid region, turtles (Ryan and Lambert, 2005; Readel et al., 2008), Northeast of Brazil. Acta Herpetologica 13: 21–32. and less is known for human environments in which Pritchard, P.C.H., Trebbau, P. (1984): The Turtles of Venezuela. these chelonians are found (Martins et al., 2010; Santana Athens, Ohio, USA, Society for the Study of Amphibians and et al., 2014, 2016). 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Accepted by Fabrício Oda