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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

  • Immunology and Host-Parasite Interactions - Original Paper
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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, and Helobdella 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.

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Acknowledgments

Santana is supported by a fellowship from The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We wish to thank CNPq for the research fellowship to DOM. Specimens were collected with permission from Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (SISBIO no. 38724-1; date of issue: April 15, 2013).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Universidade Federal da Paraíba, Cidade Universitária, Campus I, João Pessoa, PB, 58059-900, Brazil

    Daniel O. Santana, Adonias A. M. Teixeira & Daniel O. Mesquita

  2. Laboratório de Poliquetologia (LaPol), Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Matão, travessa 14, n. 101, São Paulo, SP, 05508-090, Brazil

    Rafael Eiji Iwama

  3. Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON, M5S 2C6, Canada

    Rafael Eiji Iwama

  4. Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 2B4, Canada

    Rafael Eiji Iwama

  5. Laboratório de Estudos Herpetológicos e Paleoherpetológicos, Departamento de Biologia, Universidade Federal Rural de Pernambuco, Rua Morais Rego, s/n, Dois Irmãos, Recife, PE, 52171-900, Brazil

    Geraldo J. B. Moura

  6. Programa de Pós-graduação em Ecologia e Conservação, Universidade Federal de Sergipe, Cidade Universitária Prof. José Aloísio de Campos, São Cristóvão, SE, 49100-000, Brazil

    Renato G. Faria

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  1. Daniel O. Santana
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  2. Rafael Eiji Iwama
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  3. Adonias A. M. Teixeira
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  6. Daniel O. Mesquita
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Correspondence to Daniel O. Santana.

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Appendices

Appendix 1. Voucher list

The reference specimens can be found at Collection of Hirudinea of the Federal Rural University of Pernambuco (CH-UFRPE) under numbers Haementeria brasiliensis sensu Cordero, 1937: (CH-UFRPE29; CH-UFRPE31; CH-UFRPE39; CH-UFRPE41; CH-UFRPE47; CH-UFRPE48; CH-UFRPE49; CH-UFRPE50), Helobdella cf. adiastola: (CH-UFRPE32; CH-UFRPE40), Haementeria sp1.: (CH-UFRPE35; CH-UFRPE36; CH-UFRPE37; CH-UFRPE38; CH-UFRPE46), Haementeria sp2.: (CH-UFRPE44; CH-UFRPE45).

Appendix 2. Diagnosis of leech species

Haementeria brasiliensis sensu Cordero, 1937

Diagnose: One pair of circular eyespots; paramarginal dark spots absent on ventral and dorsal surfaces; 7–9 longitudinal rows of inconspicuous tubercles on dorsal surface; Lang’s organs absent; gonopores separated by one annulus; mid-body somite biannulate, [(a1 + a2) + (a3)]; pharyngeal bulb absent; 2 pairs of compact salivary glands; 2 pairs of mycetomes, connected to esophagus by independent ducts; 7 pairs of gastric caeca; 6 pairs of testisacs.

Remarks:Haementeria brasiliensis sensu Cordero, 1937, was originally described in Oligobdella and trasnfered to Hamenteria by Oceguera-Figueroa (2012). However, the author did not account for H. brasiliensis sensu Weber, 1915, creating a synonym problem.

Haementeri a sp1.

Diagnose: one pair of eyespots; semi-circular pigmented area on the nuchal region; one pair of paramarginal dark spots on dorsum and venter of each a2; 9 longitudinal lines of large tubercles; 1 pair of Lang’s organs on a2; gonopores separated by 1 primary annulus; mid-body somites primarily triannulate, [(a1) + (a2) + (a3)]; diffuse salivary glands; 2 pairs of spherical bacteriomes; 7 pairs of gastric caeca, first pair with an anterior ramification, last pair forming a ramified post-caeca; pre-atrial loop present; 6 pairs of testisacs.

Remarks: specimens found on this study are morphology similar to Placobdella species in Ringuelet (1985a) and Cordero (1937). However, many studies consider Placobdella to be restricted to North America, except for P. costata, in Europe (Oceguera-Figueroa 2012; Siddall et al. 2005). Specimens were identified using the proposed characters in Oceguera-Figueroa (2012).

Haementeria sp2.

Diagnose: One pair of circular eyespots; no metameric pattern of pigmentation; 4 longitudinal rows of tubercles on the dorsal surface; gonopores separated by two primary annuli; mid-body somite triannulate, [(b1 + b2) + (b3 + b4) + (b5 + b6)] on dorsal surface, [(b1 + b2) + (a2) + (b5 + b6)]; 2 pairs of compact salivary glands; 2 pairs of mycetomes, connected to esophagus by independent ducts; 7 pairs of gastric caeca; 6 pairs of testisacs.

Remarks: this species resemble Haementeria lutzi and Haementeria depressa, but the position of tubercles and details on the internal morphology do not allow a precise identification of this species. Further studies are needed to understand the taxonomic status of this species.

Helobdella cf. adiastola Ringuelet, 1972

Diagnose: One pair of eyespots, close to each other; no metameric pattern of pigmentation; no tubercles or papillae on the dorsal and ventral surface; nuchal scute on the dorsal surface; gonopores separated by 1 annulus; mid-body somite triannulates, [(a1) + (a2) + (a3)]; diffuse salivary glands; bacteriomes absent.

Remarks:H. adiastola is morphologically similar to scute-bearing species from North America and Europe (Saglam et al. 2018). Helobdella stagnalis was also reported in South America, but recent studies have suggested that this species is restricted to North America. Therefore, Iwama and Arruda (2016) suggested that the name H. adiastola should be used for South American scute-bearing specimens.

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Santana, D.O., Iwama, R.E., Teixeira, A.A.M. et al. 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. Parasitol Res 118, 913–926 (2019). https://doi.org/10.1007/s00436-019-06208-x

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