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Helminth’s assemblage of a small frog in the Brazilian semiarid: parasite-host-environment relationships

Assembleia de helmintos em uma pequena rã no semiárido brasileiro: relação parasito-hospedeiro-ambiente

ABSTRACT.

Parasite infections may contingency different aspects of the hosts’ lives, and are usually expected to directly or indirectly compromise host reproduction. However, although amphibians have historically been study models in parasite ecology, the effects of parasitism on amphibians’ reproduction remain unknown. Thus, we investigated how the parasite load varies as a function of climatic seasonality (rainy and dry season) and intrinsic host characteristics (size and sex), as well as the relationship between parasite load and reproductive investment in males and females of a small frog (Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014) in the Brazilian semiarid region. The parasitological parameters of the studied population were not influenced by the season of the year or by the hosts’ body size, but females of P. pocoto had a higher prevalence and intensity of infection than males. The number of oocytes and the volume of the testes were not related to the parasite load, revealing that the parasitism did not negatively impact the gonadal investment in P. pocoto. Our findings suggest that short-lived species, such as the tiny Pseudopaludicola species, have a high reproductive investment independent of their parasitic interactions. In addition, this should be true mainly in those species that live in seasonally dry environments, such as P. pocoto, in which reproduction is even more constrained by the shortened and unpredictable rainy period.

KEYWORDS.
Amphibia; Pseudopaludicola; seasonality; reproductive allocation; Nematoda

RESUMO.

Assembleia de helmintos em uma pequena rã no semiárido brasileiro: relação parasito-hospedeiro-ambiente. Como infecções parasitárias podem contigenciar diversos aspectos da vida dos hospedeiros, de modo geral, espera-se que o parasitismo comprometa direta ou indiretamente a reprodução dos hospedeiros. Contudo, apesar dos anfíbios historicamente terem sido modelos de estudos em ecologia parasitária, os efeitos do parasitismo na reprodução de anfíbios permanecem incompreendidos. Neste trabalho investigamos como a carga parasitária varia em função da sazonalidade climática (período chuvoso e seco) e de características intrínsecas do hospedeiros (tamanho e sexo), bem como a relação entre a intensidade de infecção e o investimento reprodutivo em machos e fêmeas de uma pequena rã (Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014) no semiárido brasileiro. Os parâmetros parasitológicos da população estudada não foram influenciados pela estação do ano nem pelo tamanho corpóreo dos hospedeiros, mas as fêmeas de P. pocoto apresentaram maior prevalência e intensidade de infecção que os machos. A carga parasitária não foi relacionada com o número de ovócitos nem com o volume dos testículos, revelando que o parasitismo não impactou negativamente o investimento gonadal em P. pocoto. Nossos achados sugerem que espécies com baixa longevidade, como as diminutas espécies de Pseudopaludicola, apresentam um alto investimento reprodutivo independente de suas interações parasitárias. Complementarmente, isto deve ocorrer sobretudo naquelas espécies que vivem em ambientes sazonalmente secos, como P. pocoto, nos quais a reprodução é ainda mais contigenciada pela brevidade e imprevisibilidade do período chuvoso.

PALAVRAS-CHAVE.
Amphibia; Pseudopaludicola; sazonalidade; esforço reprodutivo; Nematoda

Macroparasites, such as helminths, can interact with their hosts in many different ways, which can cause severe damage, subtle injuries, or even not generate apparent disadvantages for the hosts (Poulin, 2007Poulin, R. 2007. Evolutionary ecology of parasites, 2ed. Princeton, Oxford, Princeton University Press. 360p.). These different consequences may be related to factors such as environmental conditions where interactions are established (Minchella, 1985Minchella, D. J. 1985. Host life-history variation in response to parasitism. Parasitology 90(1):205-216.), as well as intrinsic host and parasite features (Minchella, 1985Minchella, D. J. 1985. Host life-history variation in response to parasitism. Parasitology 90(1):205-216.; Galvani, A. P. 2003. Epidemiology meets evolutionary ecology. Trends in Ecology and Evolution 18(3):132-139.; Dybdahl & Storfer, 2003Dybdahl, M. F. & Storfer, A. 2003. Parasite local adaptation: red queen versus suicide king. Trends in Ecology and Evolution 18(10):523-530.; Poulin, 2007Poulin, R. 2007. Evolutionary ecology of parasites, 2ed. Princeton, Oxford, Princeton University Press. 360p.).

Parasites that live in environments with high climatic seasonality might have contingencies in terms of survival, transmissibility and reproduction (Altizer et al., 2006Altizer, S.; Dobson, A.; Hosseini, P.; Hudson, P.; Pascual, M. & Rohani, P. 2006. Seasonality and the dynamics of infectious diseases. Ecology Letters 9(4):467-484. ; Chandra & Gupta, 2007Chandra, P. & Gupta, N. 2007. Habitat preference and seasonal fluctuations in the helminthofauna of amphibian hosts of Rohilkhand zone, India. Asian Journal of Experimental Science 21(1):69-78.; Poulin, 2007Poulin, R. 2007. Evolutionary ecology of parasites, 2ed. Princeton, Oxford, Princeton University Press. 360p.). For example, in semiarid regions where rainfall is scarce, unpredictable and has high variability between years (Ab’Saber, 2003Ab’Saber, A. N. 2003. Os domínios de natureza no Brasil: potencialidades paisagísticas. São Paulo, Atêlie Editorial. 160 p.), helminths can be affected by the high risk of desiccation of eggs and larvae, as well as the unavailability of active hosts most of the time (Perry, 1999Perry, R. N. 1999. Desiccation survival of parasitic nematodes. Parasitology 119:S19-S30.; Madelaire et al., 2020Madelaire, C. B.; Franceschini, L.; Morais, D. H.; Gomes, F. R. & da Silva, R. J. 2020. Helminth parasites of three anuran species during reproduction and drought in the Brazilian semiarid Caatinga region. The Journal of Parasitology 106(3):334-340.). Thus, in these environments, rainy periods tend to be more favorable for the infection, development and reproduction of helminths (Poulin & Morand, 2000Poulin, R. & Morand, S. 2000. The diversity of parasites. The Quarterly Review of Biology 75(3):277-293.; Chandra & Gupta, 2007Chandra, P. & Gupta, N. 2007. Habitat preference and seasonal fluctuations in the helminthofauna of amphibian hosts of Rohilkhand zone, India. Asian Journal of Experimental Science 21(1):69-78.).

Aspects inherent to hosts such as size, sex and vagility can substantially influence helminth infection rates (Aho, 1990Aho, J. M. 1990. Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In: Esch G. W.; Bush, A. O. & Aho, J. M. eds. Parasite Communities: Patterns and Processes. Dordrecht, Springer, p. 157-195.; Price, 1990Price, P. W. 1990. Host populations as resources defining parasite community organization. In: Esch, G. W.; Bush, A. O. & Aho, J. M. eds. Parasite communities: patterns and processes. Dordrecht, Springer , p. 21-40.; Hamann et al., 2006Hamann, M. I.; Kehr, A. I. & González, C. E. 2006. Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis (Anura: Leptodactylidae) in two contrasting environments from northeastern Argentina. Journal of Parasitology 92(6):1171-1179.; Toledo et al., 2015Toledo, G. M.; Morais, D.; Silva, R. & Anjos, L. 2015. Helminth communities of Leptodactylus latrans (Anura: Leptodactylidae) from the Atlantic rainforest, south-eastern Brazil. Journal of Helminthology 89(2):250-254., 2018Toledo, G.; Schwartz, H.; Nomura, H.; Aguiar, A.; Velota, R.; Da Silva, R. & Anjos, L. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. Journal of Helminthology 92(4):438-444.). For example, hosts with larger body sizes tend to harbor a greater number of parasites (Poulin, 2007Poulin, R. 2007. Evolutionary ecology of parasites, 2ed. Princeton, Oxford, Princeton University Press. 360p.; Campião et al., 2015Campião, K. M.; Ribas, A. & Tavares, L. E. R. 2015. Diversity and patterns of interaction of an anuran-parasite network in a neotropical wetland. Parasitology 142(14):1751-1757. ). The impairment or inhibition of reproduction in hosts is one of the ways the parasites maintain the host in good energetic conditions (Hurd, 2001Hurd, H. 2001. Host fecundity reduction - a strategy for damage limitation? Trends in Parasitology 17(8):363-368.; Heins et al., 2004Heins, D. C.; Ulinski, B.; Johnson, J. & Baker, J. A. 2004. Effect of the cestode macroparasite Schistocephalus pungitii on the reproductive success of ninespine stickleback, Pungitius pungitius. Canadian Journal of Zoology 82(11):1731-1737. ). Thus, it is plausible to expect that parasitism can compromise the reproductive investment of hosts (Hurd, 2001Hurd, H. 2001. Host fecundity reduction - a strategy for damage limitation? Trends in Parasitology 17(8):363-368.). However, if on the one hand a reduction in fecundity can be an adverse effect of energy limitation provoked by infection. On the other hand, it can constitute a host defensive strategy, resulted of greater investment in survival at the expense of reproduction (Hurd, 2001Hurd, H. 2001. Host fecundity reduction - a strategy for damage limitation? Trends in Parasitology 17(8):363-368.).

Amphibians has been historically good study models for parasitic ecology, as they harbor a high diversity of parasites (Campião et al., 2014Campião, K. M.; Morais, D. H.; Dias, O. T., Aguiar, A.; Toledo, G.; Tavares, L. E. & Da Silva, R. J. 2014. Checklist of helminth parasites of amphibians from south America. Zootaxa 3843(1):1-93.) and many species are locally abundant and easy to sample (Duellman & Trueb, 1994Duellman, W. E. & Trueb, L. 1994. Biology of amphibians. Baltimore, The Johns Hopkins University Press. 670 p.). It is known that parasitic infections can affect anuran population dynamics (Johnson & Mackenzie, 2009Johnson, P. T. J. & McKenzie, V. J. 2009. Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in north America. In: Toledo, R. & Fried, B. eds. The Biology of Echinostomes. New York, Springer. 333p.; Vredenburg et al., 2010Vredenburg, V. T; Knapp, R. A.; Tunstall T. S. & Briggs, C. J. 2010. Dynamics of an emerging disease drive large-scale amphibian populations extinctions. Proceedings of the National Academy of Sciences 107(21):9689-9694.), with parasitological parameters that can vary ontogenetically (Campião et al., 2009Campião, K. M.; Silva, R. J. & Ferreira, V. L. 2009. Helminth parasites of Leptodactylus podicipinus (Anura: Leptodactylidae) from south-eastern Pantanal, state of Mato Grosso do Sul, Brazil. Journal of Helminthology 83(4):345-349. ; Todelo et al., 2015Toledo, G. M.; Morais, D.; Silva, R. & Anjos, L. 2015. Helminth communities of Leptodactylus latrans (Anura: Leptodactylidae) from the Atlantic rainforest, south-eastern Brazil. Journal of Helminthology 89(2):250-254.) and differ between the sexes (Van Sluys et al., 2006Van Sluys, M.; Schittini, G. M.; Marra, R. V.; Azevedo, A. R. M.; Vicente, J. J. & Vrcibradic, D. 2006. Body size, diet and endoparasites of the microhylid frog Chiasmocleis capixaba in an Atlantic Forest area of southern Bahia state, Brazil. Brazilian Journal of Biology 66(1a):107-173. ). As reproduction in amphibians is an activity with high energy demand (Wells, 2007Wells, K. D. 2007. The ecology and behaviour of amphibians. Chicago, University of Chicago Press. 1148p.), it is expected that parasitic infections may also compromise their reproductive efficiency. However, there is a relative lack of information on the general effects of parasitism on the reproductive investment of hosts (Hurd, 2001Hurd, H. 2001. Host fecundity reduction - a strategy for damage limitation? Trends in Parasitology 17(8):363-368.; Galdino et al., 2014Galdino, C. A.; Ávila, R. W.; Bezerra, C. H.; Passos, D. C.; Melo, G. C. & Zanchi-Silva, D. 2014. Helminths infection patterns in a lizard (Tropidurus hispidus) population from a semiarid neotropical area: associations between female reproductive allocation and parasite loads. The Journal of Parasitology 100(6):864-867.; Kiss et al., 2019Kiss, J.; Rádai, Z.; Rosa, M. E.; Kosztolányi, A. & Barta, Z. 2019. Seasonal changes in immune response and reproductive investment in a biparental beetle. Journal of Insect Physiology 121:1-31.), particularly for amphibians (Pröhl et al., 2013Pröhl, H.; Eulenburg, J.; Meuche, I. & Bolaños, F. 2013. Parasite infection has little effect on sexual signals and reproductive behaviour in strawberry poison frogs. Evolutionary Ecology 27(4):675-692.).

Parasitic interactions in amphibians have been more studied in wet tropical environments (Santos & Amato, 2010Santos, V. G. T. & Amato, S. B. 2010. Helminthfauna of Rhinella fernandezae(Anura: Bufonidae) from the Rio Grande do Sul coastland, Brazil: analysis of the parasite community. Journal of Parasitology 96(4):823-826.; Aguiar et al., 2015Aguiar, A.; Toledo, G. M.; Anjos, L. A. & Silva, R. J. 2015. Helminth parasite communities of two Physalaemus cuvieri Fitzinger, 1826 (Anura: Leiuperidae) populations under different conditions of habitat integrity in the Atlantic Rain Forest of Brazil. Brazilian Journal of Biology 75(4):963-968. ; Toledo et al., 2015Toledo, G. M.; Morais, D.; Silva, R. & Anjos, L. 2015. Helminth communities of Leptodactylus latrans (Anura: Leptodactylidae) from the Atlantic rainforest, south-eastern Brazil. Journal of Helminthology 89(2):250-254., 2017Toledo, G. M.; Fonseca, M. G.; Iannacone, J. A.; Callirgos, J. M. C.; Vidaurre, C. U. M. & Silva, R. J. 2017. Helminth parasites of Rhinella marina (Linnaeus, 1758) (Anura: Bufonidae) from Tarapoto, Peru. The Biologist 15(2):459-468., 2018Toledo, G.; Schwartz, H.; Nomura, H.; Aguiar, A.; Velota, R.; Da Silva, R. & Anjos, L. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. Journal of Helminthology 92(4):438-444.) than in dry tropical environments (Moretti et al., 2017Moretti, E. H.; Titon, B.; Madelaire, C. B.; Arruda, R.; Alvarez, T. & Gomes, F. R. 2017. Behavioral, physiological and morphological correlates of parasite intensity in the wild Cururu toad (Rhinella icterica). International Journal for Parasitology: Parasites and Wildlife 6(3):46-154. ; Silva et al., 2018Silva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.a; Madelaire et al., 2020Madelaire, C. B.; Franceschini, L.; Morais, D. H.; Gomes, F. R. & da Silva, R. J. 2020. Helminth parasites of three anuran species during reproduction and drought in the Brazilian semiarid Caatinga region. The Journal of Parasitology 106(3):334-340.). The Caatinga corresponds to the largest area of Tropical Dry Forest in South America (Da Silva et al., 2017Da Silva, J. M. C.; Leal, I. R. & Tabarelli, M. 2017. Caatinga: the largest tropical dry forest region in South America. Amsterdam, Springer International Publishing. 482 p.) and harbor one of the richest amphibian fauna among semiarid regions in the world (Garda et al., 2017Garda, A. A.; Stein, M. G.; Machado, R. B.; Lion, M. B.; Juncá, F. A. & Napoli, M. F. 2017. Ecology, biogeography, and conservation of amphibians of the Caatinga. In: Silva, J. M. C.; Leal, I. R. & Tabarelli, M. eds. Caatinga: The largest tropical dry forest region in South America. Cham, Springer, p. 133-150.). However, knowledge about parasitism in Caatinga anurans is basically constituted by punctual infection records (Teles et al., 2014Teles, D. A.; Cabral, M. E. S.; Araujo-Filho, J. A.; Dias, D. Q.; Ávila, R. W. & Almeida, W. O. 2014. Helminths of Leptodactylus vastus (Anura: Leptodactylidae) in an area of Caatinga, Brazil. Herpetology Notes 7:355-356., 2017Teles, D. A.; Brito, S. V.; Filho, J. A. A.; Teixeira, A. A. M.; Ribeiro, S. C.; Mesquita, D. O. & Almeida, W. O. 2017. Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), an endemic frog of the Caatinga domain of the neotropical region in Brazil. Herpetology Notes 10:525-527., 2018Teles, D. A.; Pinto, C. L. M.; Teixeira, A. A. M. & Filho, J. A. A. 2018. First report of Rhabdias sp. infecting Leptodactylus macrosternum from the Caatinga domain, neotropical region. Cuadernos de Herpetología 32(2):117-118.) and lists of helminth fauna for some host species (Teles et al., 2015Teles, D. A; Sousa, J. G. G.; Teixeira, A. A. M.; Silva, M. C.; Oliveira, R. H. & Ávila, R. W. 2015. Helminths of the frog Pleurodema diplolister (Anura, Leiuperidae) from the Caatinga in Pernambuco state, Northeast Brazil. Notes and Comments 75(1):251-253.; Alcantara et al., 2018Alcantara, E. P.; Ferreira-Silva, C.; Silva, L.; Lins, A.; Silva, J. R.; Ávila, R. W. & Morais, D. H. 2018. Helminths of Dermatonotus muelleri (Anura: Microhylidae) from northeastern Brazil. Journal of Parasitology 104(5):550-556. ; Oliveira et al., 2019Oliveira, C. R.; Ávila, R. W. & Morais, D. H. 2019. Helminths associated with threePhysalaemusspecies (Anura: Leptodactylidae) from Caatinga biome, Brazil. Acta Parasitology 64(1):205-212.). Since these semiarid environments have a marked seasonality in relation to water availability, which is a limiting factor both for amphibians (Carvalho et al., 2010Carvalho, J. E.; Navas, C. A. & Pereira, I. C. 2010. Energy and water in aestivating amphibians. In: Navas, C. A. & Carvalho, J. eds. Aestivation: progress in molecular and subcellular biology. Springer, Berlin, p. 141-170.; Madelaire & Gomes, 2016Madelaire, C. B. & Gomes, F. R. 2016. Breeding under unpredictable conditions: annual variation in gonadal maturation, energetic reserves and plasma levels of androgens and corticosterone in anurans from the Brazilian semi-arid. General and Comparative Endocrinology 228:9-16.) and for helminths (Perry, 1999Perry, R. N. 1999. Desiccation survival of parasitic nematodes. Parasitology 119:S19-S30.; Madelaire et al., 2020Madelaire, C. B.; Franceschini, L.; Morais, D. H.; Gomes, F. R. & da Silva, R. J. 2020. Helminth parasites of three anuran species during reproduction and drought in the Brazilian semiarid Caatinga region. The Journal of Parasitology 106(3):334-340.), it reinforces the need to provide information on host-parasite interactions between helminths and anurans in the Caatinga domain.

In the Brazilian semiarid region, most frogs concentrate their reproductive activities in the short rainy period of the year (Arzabe et al., 2005Arzabe, C.; Skuk, G.; Santana, G. G.; Delfim, F. R.; Lima, Y. C. C. & Abrantes, S. H. F. 2005. Herpetofauna da área de Curimataú, Paraíba. In: Araújo, F. S; Rodal, M. J. N. & Barbosa, M. R. V. eds. Análise das variações da biodiversidade do bioma Caatinga: suporte a estratégias regionais de conservação. Brasília, Ministério do Meio Ambiente, p. 259-274.; Jared et al., 2019Jared, C.; Mailho-Fontana, P. L.; Mendelson, J. & Antoniazzi, M. M. 2019. Life history of frogs of the Brazilian semi-arid (Caatinga), with emphasis in aestivation. Acta Zoologica 101(3):302-310. ). This is also the case of the tiny frog Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014, a species described in the last decade, which despite being common and widely distributed in the Brazilian semiarid region (Pereira et al., 2015Pereira, E. N.; Teles, M. J. L. & Santos, E. M. 2015. Herpetofauna em remanescente de Caatinga no Sertão de Pernambuco, Brasil [Herpetofauna in remnant of Caatinga from Sertão of Pernambuco, Brazil]. Boletim do Museu de Biologia Mello Leitão 37:37-51.; Lantyer-Silva et al., 2016Lantyer-Silva, A. S. F.; Matos, M. A.; Gogliath, M.; Marciano-Jr, E. & Nicola, P. A. 2016. New records of Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014 (Amphibia: Anura: Leptodactylidae) in the Caatinga Biome, Brazil. Check List 12(6):1-4.), has little ecological information available (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305., bSilva, C. S.; Sousa, J. G. G.; Lima, Y. F.; Ávila, R. W. & Morais, D. H. 2018b. Diet and morphological aspects of a population of Pseudopaludicola pocoto (Anura: Leptodactylidae) from Northeast Brazil. Neotropical Biology and Conservation 13(4):313-320.). The community of helminths that parasitize P. pocoto is known for only one location in the Caatinga (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.) and the relationships between its parasite load and its reproductive investment are completely unknown. In this study, we evaluated the ecological interactions between P. pocoto and its associated helminth fauna, specifically investigating: 1) how marked rainfall seasonality affects the parasitological parameters; 2) in what extension host body size and sex influence the parasite load and; 3) what are the relationships between the parasite load with the reproductive investment of females and males hosts.

MATERIAL AND METHODS

Fieldwork was carried out in Assú municipality (5°34’38”S, 36°54’30”W), a semiarid area located in the western region of the state of Rio Grande do Norte, Brazil. This macroregion is classified according to Köppen-Geiger as presenting a Warm Semiarid Climate (BSh), which may present a variation in annual precipitation from 400 to 1000 mm depending on the location, and annual average temperatures ranging between 22°C and 35°C (Da Silva et al., 2017Da Silva, J. M. C.; Leal, I. R. & Tabarelli, M. 2017. Caatinga: the largest tropical dry forest region in South America. Amsterdam, Springer International Publishing. 482 p.; INMET, 2018INMET - Instituto Nacional de Meteorologia do Brasil. 2018. Normais Climatológicas (1981/2010). Available in <Available in https://clima.inmet.gov.br/progp/0 >. Accessed on 22 May 2021.
https://clima.inmet.gov.br/progp/0...
). The Brazilian semiarid region is characterized by high temperatures and seasonal rains, with short rainy periods of three to four months, with unpredictable rainfall, and the dry season lasting from 7 to 10 months (Da Silva et al., 2017Da Silva, J. M. C.; Leal, I. R. & Tabarelli, M. 2017. Caatinga: the largest tropical dry forest region in South America. Amsterdam, Springer International Publishing. 482 p.). Assú municipality has historicaly an average annual precipitation of 587.4 mm, with a concentration of rainfall between February and May, whist September use to be the driest month in the region (Medeiros et al., 2005Medeiros, J. D. F.; Santos, N. C. F.; Guedes, F. X. & Santos, M. F. 2005. Análise da Precipitação e do escoamento superficial na bacia hidrográfica do rio Piranhas-Açu/RN. Natal, EMPARN, documento 29. 32p.).

We sampled specimens of Pseudopaludicola pocoto through active searches along breeding sites (Scott Jr & Woodward, 1994Scott Jr, N. J. & Woodward, B. D. 1994. Surveys at breeding sites. In: Heyer, W. R.; Donnelly, M. A.; Mcdiarmid, R. W; Hayek, L. C. & Foster, M. S. eds. Measuring and monitoring biological diversity. standard methods for amphibians. Washington and London, Smithsonian Institution Press, p. 118-124.). The samplings took placed in three temporary ponds, in the rainy months (March and May 2017, February, April and May 2018) and in the dry months (September and October 2017). We collect 94 individuals of Pseudopaludicola pocoto, 41 females and 53 males, including 23 collected in rainy and 71 in dry season. Individuals were manually captured and collected under licenses from Instituto Chico Mendes de Conservação da Biodiversidade (nº 58431-1 and nº 35650-1). The sampled individuals were transferred to the Laboratório de Ecologia e Comportamento Animal - LECA of the Universidade Federal Rural do Semi-Árido - UFERSA, in the municipality of Mossoró, Rio Grande do Norte state, where their body size was measured in terms of snout-vent length (SVL) with a caliper (resolution 0.01 mm). After that, the individuals were euthanized following the recommended ethical precepts (Resolução do Conselho Federal de Biologia - CFBio nº. 301/2012Resolução do Conselho Federal de Biologia - CFBio nº.301/2012, de 8 de dezembro de 2012.) and had their internal organs (gonads, lungs, stomach, small and large intestines) removed for parasite inspection. For proper fixation of the helminths, the organs were fixed in 70% alcohol at 60°C, and preserved in 70% alcohol for further screening, counting and identification. After necropsy, the individuals of P. pocoto were fixed in 10% formalin, preserved in 70% alcohol and deposited in the Coleção Herpetológica do Semiárido - CHSA at UFERSA (CHSA.A 642, 665, 681, 683-687, 700-708, 710-715, 726-732, 744-750, 755-766, 786-811, 813-816, 990, 1041-1047 and 1055-1061).

For taxonomic identification, the parasites were clarified in Lactofenol, subjected to compression between the slide and cover slip, and analyzed using an optical microscope. We identified the parasite specimens at the lowest possible taxonomic level according to Bacher & Vaucher (1985Bacher, M. R. & Vaucher, C. 1985. Parasitic helminths from Paraguay VII: Systematic position of Oxyascaris Travassos, 1920 (Nematoda: Cosmocercoidea). Revue Suisse de Zoologie 92(2):303-310.), Vicente et al. (1991Vicente, J. J.; Rodrigues, H. O.; Gomes, D. C. & Pinto, R. M. 1991. Nematóides do Brasil 2ª parte: nematóides de anfíbios. Revista Brasileira de Zoologia 7(4):549-626.) and, Mordeglia & Digiani (1998Mordeglia, C. & Digiani, M. C. 1998. Cosmocerca parva Travassos, 1925 (Nematoda: Cosmocercidae) in toads from Argentina. Memórias do Instituto Oswaldo Cruz 93(6):737-738.). Twenty-seven helminths could not be identified because they were diagnose structures were damaged, but were included in general parasitological metrics. We calculate the total prevalence rate (%); the mean intensity of infection and mean abundance following Bush et al. (1997Bush, A. O.; Lafferty, K. D.; Lotz, J. M. & Shostak, A. W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83(4):575-583.). These values were calculated separately by infection site, host sex and climatic season. All the helminths recorded belong to Rhabditida (Schoch et al., 2020Schoch, C. L.; Ciufo, S.; Domrachev, M.; Hotton, C. L.; Kannan, S.; Khovanskaya, R.; Leipe, D.; Mcveigh, R.; O’Neill, K.; Robbertse, B.; Sharma, S.; Soussov, V.; Sullivan, J. P.; Sun, L.; Turner, S. & Karsch-Mizrachi, I. 2020. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford). baaa062. PubMed: 32761142, PMC: PMC7408187.), feeding through valves in the esophageal bulb (Anderson, 2000Anderson, R. C. 2000. Nematode parasites of vertebrates. Their development and transmission. 2ed CABI Publishing, Wallingford, Oxon (UK). 650 p.). Thus, in view of the similar mechanisms of these parasites interact with the hosts, we consider the total number of helminths per host as the proxy to parasite load.

The reproductive investment of females was measured in terms of the total number of post-vitellogenic (mature) oocytes, those oocytes collored with a dark brown animal pole and a milky vegetative pole (Perotti, 1997Perotti, M. G. 1997. Modos reproductivos y variables reproductivas cuantitativas de un ensamble de anuros del Chaco semiárido, Salta, Argentina. Revista Chilena de História Natural 70(2):277-288.; Melchiors et al., 2004Melchiors, J.; Di-Bernardo, M.; Pontes, G. M. F.; Oliveira, R. B.; Solé, M. & Kwet, A. 2004. Reprodução de Pseudis minuta (Anura, Hylidae) no sul do Brasil. Phyllomedusa 3(1):61-68.). For males, we consider the mean testes volume of each individual as a proxy for reproductive investment (Emerson, 1997Emerson, S. 1997. Testis size variation in frogs: testing the alternatives. Behavioral Ecology Sociobiology 41:227-235.). The testis volume (in mm³) was calculated using the prolate spheroid formula: V = 4/3π (L/2) (W/2)2, where “V” is the testis volume, “L” is the testis length and “W” is the testis width (Anjos & Rocha, 2008Anjos, L. A. & Rocha, C. F. D. 2008. Reproductive ecology of the invader species gekkonid lizard Hemidactylus mabouia in an area of southeastern Brazil. Iheringia, Série Zoologia 98(2):205-209. ). We measured the width and length of each testis using a digital caliper (resolution 0.01 mm). Twenty-eight specimens of P. pocoto were excluded from this analysis as they did not have mature oocytes or the testes were degraded.

To investigate the factors affecting the parasite load, we performed a model selection by simplification of a full generalized linear model (GLM), considering a Poisson error distribution of the response variable (parasite load; i.e. the total number of parasites per host, including zeros) and all interactions between explanatory variables: snout-vent length (in mm), sampling period (rainy and dry season), and sex (female or male). To evaluate the possible negative effects of parasite load on reproductive investment, we first searched for influence of host body size (SVL) on the response variables (log transformed number of oocytes and raw testis volume) using Simple Linear Regressions (SLR). When a significant relationship was found (only in males, see results), we extracted the residuals from the regression model for further analysis. So, we made one sided Spearman's Correlations (SC) between parasite load (the total number of parasites per host, including zeros) and gonads' parameters (log transformed number of oocytes for females, and residuals from testis volume~SVL regression model for males). Prior to analysis, we evaluated the datasets regarding premises of homoscedasticity and error distributions. Whenever possible, we transformed the response variable for the use of parametric tests. All statistical analyses were conducted in R environment v.3.6.1 (R Core Team 2019R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing.), considering a significance level α = 0.05, and using the package “beeswarm” v.0.2.3 (Eklund, 2016Eklund, A. 2016. Beeswarm: The bee swarm plot, an alternative to stripchart. R package version 0.2.3. Available at <https://CRAN.R project.org/package=beeswarm>.
https://CRAN.R project.org/package=beesw...
) for graphical purposes. Descriptive characterization of variables was provided as mean ± one standard error.

RESULTS

We found a total of 91 helminths in Pseudopaludicola pocoto, and the mean intensity of infection (MII) was 1.78 ± 0.18 parasites per host. We recorded at least one helminth for 51 hosts, representing 54% of total prevalence.

The host population was infected by three nematodes species: Cosmocerca parva Travassos, 1925 (13 males and 6 females) (Cosmocercidae), Physaloptera sp. (8 larvae) (Physalopteridae), and Oxyascaris sp. (37 females) (Oxyascarididae) (Tab. I). In most of the infected hosts (86%), we found only one species of helminth, with no host harboring all three species simultaneously. The highest prevalence of helminths was in the digestive tract, mainly in small intestine (38%), followed by large intestine (14%) and stomach (12%). The small intestine was parasitized by Oxyascaris sp. (64%), C. parva (27%) and Physaloptera sp. (9%), the stomach by C. parva (67%) and Physaloptera sp. (33%), and the large intestine only by Oxyascaris sp. Only one individual of Physaloptera sp. was found in body cavity, and no lungs or gonads were infected. Regarding mean intensity of infection by site, large intestine was more infected (MII = 1.69; n = 13) than small intestine (MII = 1.53; n = 36) and stomach (MII = 1.09; n = 11) (Tab. I).

Tab. I.
Helminth assemblage associated with Pseudopaludicola pocoto (Anura, Leptodactylidae) (n = 51 frogs) from the municipality of Assú, Rio Grande do Norte State, Brazil. HN, total number of hosts per parasite species; PN, total number of nematode parasites; TPR, total prevalence rate (%); MII, mean intensity of infection, MA = mean abundance and IS = infection site (St, stomach; SI, small intestine; LI, large intestine; Cav, body cavity).

Concerning the infection patterns along the time, 56% of hosts were infected in rainy season with a mean intensity of infection of 1.38 ± 0.22, while in the dry season the prevalence was 53% with mean intensity of infection of 1.92 ± 0.16. In relation to intersexual differences, 61% of females (SVL 13.19 ± 0.14 mm) and 49% of males (SVL 11.81 ± 0.21 mm) were infected, with a mean intensity of infection of 2.04 ± 0.26 for females and 1.53 ± 0.10 for males. The overall parasite load was not influenced by body size nor sampling period, and the minimal adequate model had only host sex as the unique significant parameter (GLM - Z = -2.37; p = 0.02; Fig. 1).

Fig. 1.
Parasite load (total number of helminths per host) between females (N= 41) and males (N= 53) of Pseudopaludicola pocoto (Anura) from Assú municipality, Rio Grande do Norte state, northeastern Brazil.

Regarding influence of parasite load on reproductive investment, we considered 32 females and 34 males for which number of oocytes and testes volume were respectively quantified. The number of oocytes was not influenced by body size (SLR - R² = 0.01; p = 0.60), and the parasite load was not negatively correlated with the number of oocytes (SC - r = 0.03; p = 0.57). The mean testes volume was positively affected by body size (SLR - R² = 0.11; p = 0.05), but the parasite load was not negatively correlated the testis volume after removed the effects of body size (SC - r = - 0.15; p = 0.20).

DISCUSSION

Nematode parasites are most commonly found in frogs of the Leptodactylidae (Campião et al., 2014Campião, K. M.; Morais, D. H.; Dias, O. T., Aguiar, A.; Toledo, G.; Tavares, L. E. & Da Silva, R. J. 2014. Checklist of helminth parasites of amphibians from south America. Zootaxa 3843(1):1-93.), with eight species previously known to parasitize Pseudopaludicola pocoto (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.). We recorded three species of Nematoda parasitizing P. pocoto in in Assú municipality, Rio Grande do Norte state. Cosmocerca parva is widely distributed in South American anurans (Campião et al., 2014Campião, K. M.; Morais, D. H.; Dias, O. T., Aguiar, A.; Toledo, G.; Tavares, L. E. & Da Silva, R. J. 2014. Checklist of helminth parasites of amphibians from south America. Zootaxa 3843(1):1-93.) and has previously been reported to parasitize other Caatinga amphibians (Oliveira et al., 2019Oliveira, C. R.; Ávila, R. W. & Morais, D. H. 2019. Helminths associated with threePhysalaemusspecies (Anura: Leptodactylidae) from Caatinga biome, Brazil. Acta Parasitology 64(1):205-212.), including P. pocoto (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.). Oxyascaris sp. and Physaloptera sp. recorded by us in P. pocoto could not be identified at the species level, as there were only females of Oxyascaris sp. (diagnostic characters in males - (Bacher & Vaucher, 1985Bacher, M. R. & Vaucher, C. 1985. Parasitic helminths from Paraguay VII: Systematic position of Oxyascaris Travassos, 1920 (Nematoda: Cosmocercoidea). Revue Suisse de Zoologie 92(2):303-310.) and larvae of Physaloptera sp. (anurans are intermediate hosts - Boquimpani-Freitas et al., 2001Boquimpani-Freitas, L.; Vrcibradic, D.; Vicente, J. J.; Bursey, C. R.; Rocha, C. F. & Van Sluys, M. 2001. Helminths of the horned leaf frog, Proceratophrys appendiculata, from southeastern Brazil. Journal of Helminthology 75(3):233-236.). The total prevalence observed in Assú population was similar to that found for another population of P. pocoto located 400 km away (50% in Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305. and 54% in the present study). However, we observed a higher mean intensity of infection in the study area (MII = 1.8 ± 1.3 parasites/host) than that previously recorded for another population (MII = 1.0 ± 0.5 parasite/host) (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.). As other species of Oxyascaris and Physaloptera have also been reported to parasitize P. pocoto (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.), our results suggest that the helminth fauna composition in P. pocoto may not vary substantially between populations.

The prevalence and mean intensity of infection in P. pocoto did not differ between the rainy and dry seasons. In semiarid regions, it is expected that the activity of most frogs is restricted to the short rainy period of the year, when reproduction is concentrated (Abe, 1995Abe, A. S. 1995. Estivation in south American amphibians and reptiles. Brazilian Journal of Medical and Biological Research 28(11/12):1241-1247.; Garda et al., 2017Garda, A. A.; Stein, M. G.; Machado, R. B.; Lion, M. B.; Juncá, F. A. & Napoli, M. F. 2017. Ecology, biogeography, and conservation of amphibians of the Caatinga. In: Silva, J. M. C.; Leal, I. R. & Tabarelli, M. eds. Caatinga: The largest tropical dry forest region in South America. Cham, Springer, p. 133-150.). We expected that the number of parasites per host would be greater during the reproductive period (Filho et al., 2016Filho, J. A.; Brito, S. V.; Lima, V. F.; Pereira, A. M.; Mesquita, D. O.; Albuquerque, R. L. & Almeida, W. O. 2016. Influence of temporal variation and host condition on helminth abundance in the lizard Tropidurus hispidus from north-eastern Brazil. Journal of Helminthology 91(3):312-319.; Oliveira et al., 2017Oliveira, B. H. S.; Teixeira, A. A. M.; Queiroz, R. N. M.; Araujo-Filho, J. A.; Teles, D. A.; Brito, S. V. & Mesquita, D. O. 2017. Nematodes infecting Anotosaura vanzolinia (Squamata: Gymnophthalmidae) from Caatinga, northeastern Brazil. Acta Herpetologica 12(1):103-108. ), when the majority of anurans are active and, consequently, they would be more exposed to infection by parasites (Poulin & Morand, 2000Poulin, R. & Morand, S. 2000. The diversity of parasites. The Quarterly Review of Biology 75(3):277-293.). However, as observed in another population (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.), we also recorded some P. pocoto individuals active in the first months of dry period next to remaining water bodies. In this sense, it is known that anuran species that have a prolonged period of activity tend to have prevalence and infection rates more distributed over time (Madelaire et al., 2020Madelaire, C. B.; Franceschini, L.; Morais, D. H.; Gomes, F. R. & da Silva, R. J. 2020. Helminth parasites of three anuran species during reproduction and drought in the Brazilian semiarid Caatinga region. The Journal of Parasitology 106(3):334-340.). Thus, although the reproductive activity of Pseudopaludicola species are considered explosive, it is possible that P. pocoto behaves in an opportunistic way, taking advantage of fortuitous favorable conditions between years according to rainfall distribution. If this is true, this strategy could explain the low variation observed in the parasitological parameters of P. pocoto between the rainy and dry periods.

The body size of P. pocoto was not related to the parasite load. However, it is known that the body size of the host is in general positively related to the richness and abundance of parasites, both because large species have a greater capacity for ingesting prey, and because they have a larger surface area and body volume for colonization by helminths (Campião et al., 2015Campião, K. M.; Ribas, A. & Tavares, L. E. R. 2015. Diversity and patterns of interaction of an anuran-parasite network in a neotropical wetland. Parasitology 142(14):1751-1757. ; Toledo et al., 2018Toledo, G.; Schwartz, H.; Nomura, H.; Aguiar, A.; Velota, R.; Da Silva, R. & Anjos, L. 2018. Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. Journal of Helminthology 92(4):438-444.). Our results suggest that the low variation in body size of P. pocoto individuals is not enough to enable a significantly higher number of parasites in larger hosts. It is noteworthy that the widely known pattern of sexual dimorphism for anurans, in which females are larger than males (Duellman & Trueb, 1994Duellman, W. E. & Trueb, L. 1994. Biology of amphibians. Baltimore, The Johns Hopkins University Press. 670 p.), is not observed in P. pocoto (Silva et al., 2018bSilva, C. S.; Sousa, J. G. G.; Lima, Y. F.; Ávila, R. W. & Morais, D. H. 2018b. Diet and morphological aspects of a population of Pseudopaludicola pocoto (Anura: Leptodactylidae) from Northeast Brazil. Neotropical Biology and Conservation 13(4):313-320.), contributing to explain the lack of relationship between body size and parasite load. In fact, Pseudopaludicola species are recognized by their small body size, a characteristic that can restrict the parasite load independent of intraspecific variation in body size (Duré et al., 2004Duré, M. I.; Schaefer, E. F.; Hamann, M. I. & Kehr, A. I. 2004. Consideraciones ecológicas sobre la dieta, la reproducción y el parasitismo de Pseudopaludicola boliviana (Anura, Leptodactylidae) de Corrientes, Argentina. Phyllomedusa 3(2):121-131.).

Sex significantly influenced the parasite load in P. pocoto, with the number of parasitized females 10% higher than those of males and with females harboring 30% more parasites than males. Although in general amphibians have low vagility compared to other vertebrates (Wells, 2007Wells, K. D. 2007. The ecology and behaviour of amphibians. Chicago, University of Chicago Press. 1148p.), females occasionally travel longer distances than males (Wells, 2007Wells, K. D. 2007. The ecology and behaviour of amphibians. Chicago, University of Chicago Press. 1148p.; Wang et al., 2019Wang, W.; Wei, S.; Chen, M. & Wu, H. 2019. Female-biased dispersal of the Emei Moustache toad (Leptobrachium boringii) under Local resource competition. Asian Herpetological Research 10(1):24-31.). This displacement may be related to greater foraging/feeding intensity to offset the greater energy demands for oocyte production (Price, 1990Price, P. W. 1990. Host populations as resources defining parasite community organization. In: Esch, G. W.; Bush, A. O. & Aho, J. M. eds. Parasite communities: patterns and processes. Dordrecht, Springer , p. 21-40.; Muths, 2003Muths, E. 2003. Home range and movements of boreal toads in undisturbed habitat. Copeia 2003(1):160-165.). Thus, it is possible that females of P. pocoto are doubly more susceptible to infection by helminths, both because of the possible greater vagility in search of prey (cutaneous infection route - Poulin, 2007Poulin, R. 2007. Evolutionary ecology of parasites, 2ed. Princeton, Oxford, Princeton University Press. 360p.), and because they feed on a greater diversity of prey (infection oral route - Poulin, 2007Poulin, R. 2007. Evolutionary ecology of parasites, 2ed. Princeton, Oxford, Princeton University Press. 360p.; Leivas et al., 2018Leivas, P. T.; Leivas, F. W. T. & Campião, K. 2018. Diet and parasites of the anuran Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) from an Atlantic Forest fragment. Herpetology Notes 11:109-113.). Since the only study on the foraging ecology of P. pocoto did not assess the intersexual differences in diet (see Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.), we recommend future studies on this topic to test the aforementioned predictions.

Hosts with a higher parasite load may present reproductive contingencies (Minchella, 1985Minchella, D. J. 1985. Host life-history variation in response to parasitism. Parasitology 90(1):205-216.; Hurd, 2001Hurd, H. 2001. Host fecundity reduction - a strategy for damage limitation? Trends in Parasitology 17(8):363-368.; Bower et al., 2018Bower, D. S.; Brannelly, L. A.; McDonald, C. A.; Webb, R. J.; Greenspan, S. E.; Vickers, M.; Gardner, M. G. & Greenlees, M. J. 2018. A review of the role of parasites in the ecology of reptiles and amphibians. Austral Ecology 44(3):433-448. ), but the reproductive investment of P. pocoto was not affected by the parasite load. It is known that anuran species with small body size tend to live shorter than larger ones (Duellman & Trueb, 1994Duellman, W. E. & Trueb, L. 1994. Biology of amphibians. Baltimore, The Johns Hopkins University Press. 670 p.; Stark & Meiri, 2018Stark, G. & Meiri, S. 2018. Cold and dark captivity: drivers of amphibian longevity. Global Ecology and Biogeography 27(11):1384-1397.). Consequently, despite the trade-off between growing and reproducing, short-lived species are expected to have a relatively higher reproductive investment (Scharf et al., 2015Scharf, I.; Feldman, A.; Novosolov, M.; Pincheira‐Donoso, D.; Das, I.; Böhm, M.; Uetz, P.; Torres‐Carvajal, O.; Bauer, A.; Roll, U. & Meiri, S. 2015. Late bloomers and baby boomers: ecological drivers of longevity in squamates and the tuatara. Global Ecology and Biogeography 24(4):396-405.). Thus, it is possible that the species of Pseudopaludicola, among the smallest representatives of the Leptodactylidae (Giaretta & Kokobum, 2003Giaretta, A. A. & Kokobum, M. N. 2003. A new species of Pseudopaludicola (Anura, Leptodactylidae) from northern Brazil. Zootaxa 383(1):1-8.; Andrade et al., 2016Andrade, F. S.; Magalhães, F. M.; Nunes-De-Almeida, C. H. L.; Veiga-Menoncello, A. C. P.; Santana, D. J.; Garda, A. A.; Loebmann, D.; Recco-Pimentel, S. M.; Giaretta, A. A. & Toledo, L. F. 2016. A new species of long-legged Pseudopaludicola from northeastern Brazil (Anura, Leptodactylidae, Leiuperinae). Salamandra 52(2):107-124. , 2020Andrade, F. S.; Haga, I. A.; Lyra, M. L.; Carvalho, T. R.; Haddad, C. F. B.; Giaretta, A. A. & Toledo, L. F. 2020. Reassessment of the taxonomic status of Pseudopaludicola parnaiba (Anura, Leptodactylidae, Leiuperinae), with the description of a new cryptic species from the Brazilian Cerrado. European Journal of Taxonomy 679:1-36.; Pansonato et al., 2016Pansonato, A.; Veiga-Menoncello, A. C. P.; Mudrek, J. R.; Jansen, M.; Recco-Pimentel, S. M.; Martins, I. A. & Strüssmann, C. 2016. Two new species of Pseudopaludicola (Anura: Leptodactylidae: Leiuperinae) from eastern Bolivia and western Brazil. Herpetologica 72(3):235-255.), have a low longevity and may present a high reproductive investment independent of their parasitic interactions (Silva et al., 2018aSilva, C. S.; Ávila, R. W. & Morais, D. H. 2018a. Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from Northeast-Brazilian. Helminthologia 55(4):292-305.,bSilva, C. S.; Sousa, J. G. G.; Lima, Y. F.; Ávila, R. W. & Morais, D. H. 2018b. Diet and morphological aspects of a population of Pseudopaludicola pocoto (Anura: Leptodactylidae) from Northeast Brazil. Neotropical Biology and Conservation 13(4):313-320.).

Although parasitic infections are often related to the damage of hosts (Agnew et al., 2000Agnew, P.; Koella, J. C. & Michalakis, Y. 2000. Host life history responses to parasitism. Microbes and Infection 2(8):891-896.; Galdino et al., 2014Galdino, C. A.; Ávila, R. W.; Bezerra, C. H.; Passos, D. C.; Melo, G. C. & Zanchi-Silva, D. 2014. Helminths infection patterns in a lizard (Tropidurus hispidus) population from a semiarid neotropical area: associations between female reproductive allocation and parasite loads. The Journal of Parasitology 100(6):864-867.; Moretti et al., 2017Moretti, E. H.; Titon, B.; Madelaire, C. B.; Arruda, R.; Alvarez, T. & Gomes, F. R. 2017. Behavioral, physiological and morphological correlates of parasite intensity in the wild Cururu toad (Rhinella icterica). International Journal for Parasitology: Parasites and Wildlife 6(3):46-154. ), this pattern did not occur in a P. pocoto population from Caatinga. As an environment with a short and unpredictable rainy season, the semiarid is known to exert an even greater contingency for the reproduction of amphibians, and may frame specific ecological and behavioral strategies (Madelaire & Gomes, 2016Madelaire, C. B. & Gomes, F. R. 2016. Breeding under unpredictable conditions: annual variation in gonadal maturation, energetic reserves and plasma levels of androgens and corticosterone in anurans from the Brazilian semi-arid. General and Comparative Endocrinology 228:9-16.). For example, it has been suggested in last years that amphibians from semiarid regions have a relatively more intense immune response, contributing so that parasitic diseases do not cause substantial damage to reproduction (Madelaire et al., 2017Madelaire, C. B.; Sokolova, I. & Gomes, F. R. 2017. Seasonal patterns of variation in steroid plasma levels and immune parameters in anurans from Brazilian semiarid area. Physiological and Biochemical Zoology 90(4):415-433.). In conclusion, keeping in mind that the patterns of the host's life history and their relationships with the environment can act as mediators of physiological responses to parasitism (Minchella, 1985Minchella, D. J. 1985. Host life-history variation in response to parasitism. Parasitology 90(1):205-216.), our findings contribute to the understanding of the consequences of parasitic interactions in amphibians, revealing the nature of parasitism by nematodes in a small frog from a semiarid environment.

Acknowledgments

We thank Anyssa Oliveira, Eduarda Lima-Alves, Nilton Aquino and Paulo Cunha for assistance in the fieldwork and laboratory analysis; Camila Kamblevicius for help to parasites identification. We are grateful to Castiele Bezerra and José Luís Novaes for valuable suggestions to a prior version of this manuscript. P.B.S. thanks the Universidade Federal Rural do Semi-Árido - UFERSA and the Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for undergraduate scholarship of scientific initiation.

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Publication Dates

  • Publication in this collection
    05 Sept 2022
  • Date of issue
    2022

History

  • Received
    20 Oct 2021
  • Accepted
    03 June 2022
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