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Phrynops Geoffroanus and Mesoclemmys Tuberculata in Areas of the Caatinga and Atlantic Forest in Northeast Brazil

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Phrynops Geoffroanus and Mesoclemmys Tuberculata in Areas of the Caatinga and Atlantic Forest in Northeast Brazil Parasitology Research (2019) 118:913–926 https://doi.org/10.1007/s00436-019-06208-x IMMUNOLOGY AND HOST-PARASITE INTERACTIONS - ORIGINAL PAPER Spatio-temporal variation and the use of host body surface by ectoparasites of the chelonians Phrynops geoffroanus and Mesoclemmys tuberculata in areas of the Caatinga and Atlantic Forest in northeast Brazil Daniel O. Santana1 & Rafael Eiji Iwama2,3,4 & Adonias A. M. Teixeira1 & Geraldo J. B. Moura5 & Renato G. Faria6 & Daniel O. Mesquita1 Received: 22 February 2018 /Accepted: 10 January 2019 /Published online: 9 February 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Ectoparasites such as hematophagous leeches and monogeneans are common in chelonians, occupying different parts of the body. Thus, the present study aimed to identify and describe the fauna of ectoparasites that infest Phrynops geoffroanus and Mesoclemmys tuberculata to evaluate the effect of host conditions and seasonality (dry and rainy season) on the abundance and composition of ectoparasites. We verified the presence of ectoparasites in 73.2% of the examined turtles, with four species of leeches belonging to Glossiphoniidae, Haementeria brasiliensis sensu Cordero, 1937, Helobdella cf. adiastola, Haementeria sp1., and Haementeria sp2., and one monogenean Polystomatidae, Polystomoides brasiliensis. For both chelonians, we observed a significant difference in the abundance of ectoparasites in relation to sex, biome, and season, which was unrelated to length and mass. Leeches were more frequent in the cavities of the hind limbs in P.geoffroanus, and the anterior limbs of M. tuberculata.The general spatial niche overlap of ectoparasites was high, except for that of the monogenean P. brasiliensis, which did not overlap with those of other leech species. The present study is the first report of the presence of H. brasiliensis and P. brasiliensis parasitizing M. tuberculata,andHelobdella cf. adiastola in a phoretic relationship with P. geoffroanus and M. tuberculata. Finally, the differences in infestation levels may reflect ecological factors, differences in behavioral patterns of the hosts, and different anthropic alterations suffered in the Caatinga and Atlantic Forest biomes. Keywords Hirudinea . Leeches . Monogenae . Niche breadth . Overlap . Host Introduction conservation studies concerning issues relating to population health, including parasitism, is increasing (Meffe 1999;Deem Parasites potentially affect the life history of their hosts et al. 2001). Parasitism and with predation and competition act (Møller et al. 1990; Møller et al. 2003). The number of as great selective forces in the evolution of the species and are Handling Editor: Bill Chobotar * Daniel O. Santana 4 Department of Ecology and Evolutionary Biology, University of [email protected] Toronto, 25 Willcocks Street, Toronto, ON M5S 2B4, Canada 5 Laboratório de Estudos Herpetológicos e Paleoherpetológicos, 1 Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Departamento de Biologia, Universidade Federal Rural de Universidade Federal da Paraíba, Cidade Universitária, Campus I, Pernambuco, Rua Morais Rego, s/n, Dois Irmãos, João Pessoa, PB 58059-900, Brazil Recife, PE 52171-900, Brazil 6 2 Laboratório de Poliquetologia (LaPol), Departamento de Zoologia, Programa de Pós-graduação em Ecologia e Conservação, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Universidade Federal de Sergipe, Cidade Universitária Prof. José Matão, travessa 14, n. 101, São Paulo, SP 05508-090, Brazil Aloísio de Campos, São Cristóvão, SE 49100-000, Brazil 3 Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6, Canada 914 Parasitol Res (2019) 118:913–926 responsible for population and community structure (Gibbons the diversity of leeches and that no major studies on Brazilian et al. 2000; Menezes 2000;SilvaandAraújo2008). However, leech fauna have been conducted. Despite their ecological poten- little is known about the dynamics of parasites in natural popu- tial as bioindicator organisms, basic studies on the taxonomy, lations of reptiles, especially freshwater turtles (Ryan and biology, and ecology of leeches are practically neglected in trop- Lambert 2005;Readeletal.2008). Moreover, ectoparasites like ical regions (Christoffersen 2007; Iwama and Arruda 2016). In hematophagous leeches are common in aquatic turtles (Ringuelet addition, despite being important components of benthic com- 1944b;Sawyer1986;Watermolen1996; Light and Siddall 1999; munities, they are often not properly identified and included in Siddall and Borda 2004; Cubas et al. 2006), usually occupying the analysis of macroinvertebrates (Gullo 2014). the pleural cavity of the arms, legs, neck, tail, and even the mouth Monogeneans are parasites of mainly semi-aquatic and aquat- (Jacobson et al. 1989;Herbst1994). ic vertebrates, principally fish (Reichenbach-Klinke 1966), but Leeches are known environmental bioindicators (Sawyer are also found in amphibians (Yamaguti 1963), mammals 1986;Christoffersen2007). The high degree of endemism of (Stunkard 1924), and freshwater and marine turtles (Platt 2000; aquatic leeches makes them potentially useful as indicator spe- Ávila et al. 2010; Domènech et al. 2016). cies of water quality and undisturbed environments, since their Polystomatidae (Monogenea) are found exclusively parasitiz- habitat specificity makes them very sensitive to any form of ing chelonians, often infecting the conjunctival sac, urinary blad- anthropic influence (Christoffersen 2007). Koperski (2005)also der, and oral cavity (Du Preez and Lim 2000;Platt2000;Ávila emphasizes that the Hirudinea present a low level of mobility, et al. 2010; Du Preez and Van Rooyen 2015;Domènechetal. high degree of oxygen absorption, and low diversity in compar- 2016). We know little about the life cycle of these parasites, and ison with other invertebrates, attributes that strengthen their po- most of the scarcely available information summarizes records of sition as bioindicators of environmental quality. However, some hosts and sites of infestation. For example, only recently was a studies have reported a relationship between the occurrence of monogenean, Polystomoides brasiliensis Vieira et al., 2008, de- leeches and levels of organic pollutants, physical-chemical fac- scribed in chelonians in Brazil (Vieira et al. 2008). tors of water and food availability (Sawyer 1986; Miserendino Parasitism by leeches has been reported in Phrynops and Gullo 2014; Brites and Rantin 2004), considering that in geoffroanus (Schweigger, 1812) (Ringuelet 1981; Brites and some cases, these factors could promote even more damage to Rantin 2004;Ferronatoetal.2009), and the presence of hosts, as they can favor attack by parasites, leading to large monogenoids P. brasiliensis and Polystomoides sp. has been infestations (Brites and Rantin 2004). recorded (Vieira et al. 2008). Information related to ectopara- The Hirudinea, in addition to being parasites, are important sites of Mesoclemmys tuberculata (Lüderwaldt, 1926) is un- components of the benthic macroinvertebrates of rivers and available at this time. streams and is a taxon with a remarkable degree of endemism The objective of this study was to identify and describe the in the Neotropical region (Ringuelet 1944a; Christoffersen fauna of ectoparasites that infest P. geoffroanus and 2009). With the exception of some cosmopolitan species, the vast M. tuberculata, to evaluate the effect of host conditions (maxi- majority have a relatively low dispersion capacity (Ringuelet mum carapace length (CL) and body mass), sex, and seasonality 1944b;Gullo2014), which provides a great diversity of endemic (dry and rainy season) on the abundance and composition of species (Siddall and Borda 2004;Christoffersen2007, ectoparasites. We also describe patterns in the use of the micro- Christoffersen 2008). habitat (body surfaces of the chelonians) and the differences Seven families of aquatic leeches are present in the found in fixation site preference between ectoparasites and com- Neotropical region: Glossiphoniidae (Vaillant, 1890), Psicolidae pare infestation rates in each host between the different biomes (Johnson, 1965), Ozobranchidae (Pinto, 1921), Cilicobdellidae occurring in environments of the Caatinga and Atlantic forest in (Ringuelet, 1972), Semiscolecidae (Scriban and Autrum, 1934), an area of northeastern Brazil. Praobdellidae (Sawyer, 1986), and Macrobdellidae (Richardson, 1969) (Soós 1970; Christoffersen 2008; César et al. 2009; Christoffersen 2009; Phillips et al. 2010). Glossiphoniidae com- Materials and methods prises the largest family in number of freshwater species, includ- ing predatory species of macroinvertebrates and the temporal Study sites ectoparasites of fish, turtles, amphibians, mammals, and even aquatic birds (Ringuelet 1985a;Sawyer1986; Oceguera- Samples of P. geoffroanus and M. tuberculata were obtained Figueroa 2012). In the Neotropical region, studies of the biodi- from six localities, three in the Caatinga, and three in the versity of Hirudinea are scarce (Ringuelet 1944b, 1981, 1985a; Atlantic Forest in the State of Sergipe, Brazil (Fig. 1). The se- Gullo 1998; Christoffersen 2007;Gullo2007; César et al. 2009; lected locations in the Caatinga area were the Monumento Christoffersen 2009), and no natural history information is avail- Natural do Rio São Francisco (09°41.202′ S, 037°42.963′ W— able for freshwater environments (Gullo 2014). Iwama and municipality of Poço Redondo),
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