Helminth fauna of Norops fuscoauratus (D’Orbigny, 1837) (Squamata: Dactyloidae) in the Atlantic Forest, northeastern Brazil

Helmintofauna de Norops fuscoauratus (D’Orbigny, 1837) (Squamata: Dactyloidae) na Mata Atlântica, Nordeste, Brasil

I. H. M. P. Campos C. N. Oliveira J. V. Araújo-Neto S. V. Brito M. C. Guarnieri S. C. Ribeiro About the authors

Abstract

The composition of macro endoparasites associated with the lizard Norops fuscoauratus (Squamata) was analysed in two localities in the Atlantic Forest on the northeast of Brazil between December 2012 and July 2015. 74 specimens of N. fuscoauratus were examined and five species of helminths were reported, being: (a) for the population of Pernambuco: Cystacanth (Prevalence=37.5%), Physaloptera retusa Rudolphi, 1819 (Prevalence=4.16%), larva of flatworm (Prevalence=2.08%), Rhabdias sp. (Prevalence=2.08%) and Strongyluris oscari Travassos, 1923 (Prevalence=2.08%), and (b) of Alagoas: S. oscari (Prevalence=17.85%) and Rhabdias sp. (Prevalence=3.57%). The differences in the composition of endoparasites in the two populations are attributed to individualities of environments occupied by the lizards. The collection period does not influence the abundance of parasites, but when associated with sex, there was a positive correlation with the abundance of helminths, with more females than males being infected with parasites in the rainy season.

Keywords:
lizards; anole; endoparasites; Pernambuco; Alagoas

Resumo

A composição de macro endoparasitas associada com o lagarto Norops fuscoauratus (Squamata) foi analisada em duas localidades da Mata Atlântica no nordeste do Brasil, entre dezembro de 2012 e julho de 2015. 74 espécimes foram examinados e cinco espécies de helmintos foram encontradas, sendo: (a) para a população de Pernambuco: Cistacanto (Prevalência=37.5%), Physaloptera retusa Rudolphi, 1819 (Prevalência=4.16%), larva de platelminto (Prevalência=2.08%), Rhabdias sp. (Prevalência =2.08%) e Strongyluris oscari Travassos, 1923 (Prevalência =2.08%) e (b) Alagoas: S. oscari (Prevalência=17.85%) e Rhabdias sp. (Prevalência =3.57%). As diferenças na composição dos endoparasitas nas duas populações pode ser atribuída as individualidades dos ambientes ocupados por esses lagartos. O período de coleta não influenciou na abundância de parasitas, mas quando associado com o sexo, houve uma correlação positiva com a abundância de helmintos, com mais fêmeas do que machos, infectadas na estação chuvosa.

Palavras-chave:
lagartos; anole; endoparasitas; Pernambuco; Alagoas

1. Introduction

The disdain for parasites is usually a result of not understanding the complex biology and ecology of these organisms, neglecting their important role in the ecosystems (Marcogliese, 2004MARCOGLIESE, D.J., 2004. Parasites: small players with crucial roles in the ecological theater. EcoHealth, vol. 1, no. 2, pp. 151-164. http://dx.doi.org/10.1007/s10393-004-0028-3.
http://dx.doi.org/10.1007/s10393-004-002...
).

Just over two decades ago, helminth fauna associated with reptiles was characterized as poor and unrepresentative (Aho, 1990AHO, J.M., 1990. Helminthes communities of amphibians and reptiles: comparative approaches to understanding patterns and process. In: G. W. ESCH, A. O. BUSH and J. M. AHO, eds. Parasite communities: patterns and process. Netherlands: Springer, pp. 157-190. http://dx.doi.org/10.1007/978-94-009-0837-6_7.
http://dx.doi.org/10.1007/978-94-009-083...
). However, Avila and Silva (2010) emphasized studies conducted in the neotropics and classified the community of macro endoparasites associated with reptiles as expressive and diverse. This diversity among brazilian lizards has been increasing considerably as new species of helminths and new hosts for known species are described (Ávila and Silva, 2010ÁVILA, R.W. and SILVA, R.J., 2010. Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. The Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 16, no. 4, pp. 543-572. http://dx.doi.org/10.1590/S1678-91992010000400005.
http://dx.doi.org/10.1590/S1678-91992010...
). Apart from the revision held by Ávila and Silva (2010)ÁVILA, R.W. and SILVA, R.J., 2010. Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. The Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 16, no. 4, pp. 543-572. http://dx.doi.org/10.1590/S1678-91992010000400005.
http://dx.doi.org/10.1590/S1678-91992010...
, other studies developed in Brazil and equally important have been published in recent years, like Anjos et al. (2011)ANJOS, L.A., BEZERRA, C.H., PASSOS, D.C., ZANCHI, D. and GALDINO, C.A.B., 2011. Helminth fauna of two gekko lizards, Hemidactylus agrius and Lygodactylus klugei (Gekkonidade), from caatinga biome, northeastern Brazil. Neotropical Helminthology, vol. 5, pp. 285-290., Ávila et al. (2012)ÁVILA, R.W., ANJOS, L.A., RIBEIRO, S.C., MORAIS, D.H., SILVA, R.J. and ALMEIDA, W.O., 2012. Nematodes of Lizards (Reptilia : Squamata) from Caatinga biome, Northeastern Brazil. Comparative Parasitology, vol. 79, no. 1, pp. 56-63. http://dx.doi.org/10.1654/4518.1.
http://dx.doi.org/10.1654/4518.1...
, Ribeiro et al. (2012)RIBEIRO, S.C., FERREIRA, F.S., BRITO, S.V., TELES, D.A., ÁVILA, R.W., ALMEIDA, W.O., ANJOS, L.A. and GUARNIERI, M.C., 2012. Pulmonary infection in two sympatric lizards, Mabuya arajara (Scincidae) and Anolis brasiliensis (Polychrotidae) from a cloud forest in Chapada do Araripe, Ceará, Northeastern Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 4, pp. 929-933. http://dx.doi.org/10.1590/S1519-69842012000500021. PMid:23295524.
http://dx.doi.org/10.1590/S1519-69842012...
, Brito et al. (2014aBRITO, S.V., CORSO, G., ALMEIDA, A., FERREIRA, F.S., ALMEIDA, W.O., ANJOS, L.A., MESQUITA, D.O. and VASCONCELLOS, A., 2014a. Phylogeny and micro-habitats utilized by lizards determine the composition of their endoparasites in the semiarid Caatinga of Northeast Brazil. Parasitology Research, vol. 113, no. 11, pp. 3963-3972. http://dx.doi.org/10.1007/s00436-014-4061-z. PMid:25096534.
http://dx.doi.org/10.1007/s00436-014-406...
, b), Araújo-Filho et al. (2014) for the populations from the semi-arid; Cabral et al. (2018)CABRAL, A.N., TELES, D.A., BRITO, S.V., ALMEIDA, W.O., ANJOS, L.A., GUARNIERI, M.C. and RIBEIRO, S.C., 2018. Helminth parasites of Mabuya arajara Rebouças-Spieker, 1981 (Lacertilia: Mabuyidae) from Chapada do Araripe, northeastern Brazil. Parasitology Research, vol. 117, no. 4, pp. 1185-1193. http://dx.doi.org/10.1007/s00436-018-5797-7. PMid:29435716.
http://dx.doi.org/10.1007/s00436-018-579...
, Amorim and Ávila (2019)AMORIM, D.M. and ÁVILA, R.W., 2019. Infection patterns of helminths in Norops Brasiliensis (Squamata, Dactyloidae) from a Humid Forest, Northeastern Brazil and their relation with body mass, sex, host size, and season. Helminthologia, vol. 56, no. 2, pp. 168-174. http://dx.doi.org/10.2478/helm-2019-0011. PMid:31662688.
http://dx.doi.org/10.2478/helm-2019-0011...
and Santos Mesquita et al. (2020)SANTOS MESQUITA, J.M., OLIVEIRA, S.S., PEREZ, R. and ÁVILA, R.W., 2020. Helminths associated with Norops fuscoauratus (Squamata, Dactyloidae) in highland marshes of the Brazilian semi-arid. Journal of Helminthology, vol. 94, no. e153, pp. 1-7. http://dx.doi.org/10.1017/S0022149X20000358. PMid:32390581.
http://dx.doi.org/10.1017/S0022149X20000...
for humid forest (“Brejos-de-altitude”) and Almeida-Gomes et al. (2012)ALMEIDA-GOMES, M., VRCIBRADIC, D., MAIA-CARNEIRO, T. and ROCHA, C.F.D., 2012. Diet and endoparasites of the lizard Gymnodactylus darwinii (Gekkota, Phyllodactylidae) from an Atlantic Rainforest area in southeastern Brazil. Biotemas, vol. 25, pp. 203-206. http://dx.doi.org/10.5007/2175-7925.2012v25n1p203.
http://dx.doi.org/10.5007/2175-7925.2012...
, Barreto-Lima et al. (2012)BARRETO-LIMA, A.F., TOLEDO, G.M. and ANJOS, L.A., 2012. The nematode community in the Atlantic rainforest lizard Enyalius perditus Jackson, 1978 from southeastern Brazil. Journal of Helminthology, vol. 86, no. 4, pp. 395-400. http://dx.doi.org/10.1017/S0022149X11000599. PMid:22008646.
http://dx.doi.org/10.1017/S0022149X11000...
and Teixeira et al. (2020)TEIXEIRA, A.A.M., RIUL, P., BRITO, S.V., ARAUJO-FILHO, J.A., TELES, D.A., ALMEIDA, W.O. and MESQUITA, D.O., 2020. Ecological release in lizard endoparasites from the Atlantic Forest, northeast of the Neotropical Region. Parasitology, vol. 147, no. 4, pp. 491-450. http://dx.doi.org/10.1017/S0031182020000025. PMid:31965954.
http://dx.doi.org/10.1017/S0031182020000...
for lizards from the Atlantic Forest. In addition to these contributions, the descriptive study by Albuquerque et al. (2012)ALBUQUERQUE, S., ÁVILA, R.W. and BERNARDE, P.S., 2012. Occurrence of Helminths in Lizards (Reptilia: Squamata) at Lower Moa River Forest, Cruzeiro do Sul, Acre, Brazil. Comparative Parasitology, vol. 79, no. 1, pp. 64-67. http://dx.doi.org/10.1654/4539.1.
http://dx.doi.org/10.1654/4539.1...
should be highlighted. This study was conducted in the Amazon rainforest as a collaboration to investigate the helminth fauna associated with lizards, including additional research on Norops fuscoauratus as the host of the nematode Physaloptera retusa. Avila and Silva (2013), Teixeira et al. (2020)TEIXEIRA, A.A.M., RIUL, P., BRITO, S.V., ARAUJO-FILHO, J.A., TELES, D.A., ALMEIDA, W.O. and MESQUITA, D.O., 2020. Ecological release in lizard endoparasites from the Atlantic Forest, northeast of the Neotropical Region. Parasitology, vol. 147, no. 4, pp. 491-450. http://dx.doi.org/10.1017/S0031182020000025. PMid:31965954.
http://dx.doi.org/10.1017/S0031182020000...
and Santos Mesquita et al. (2020)SANTOS MESQUITA, J.M., OLIVEIRA, S.S., PEREZ, R. and ÁVILA, R.W., 2020. Helminths associated with Norops fuscoauratus (Squamata, Dactyloidae) in highland marshes of the Brazilian semi-arid. Journal of Helminthology, vol. 94, no. e153, pp. 1-7. http://dx.doi.org/10.1017/S0022149X20000358. PMid:32390581.
http://dx.doi.org/10.1017/S0022149X20000...
also present important data on parasites of this lizard.

The genus Norops Wagler (1830), one of eight genera reallocated to reclassify the anole (Nicholson et al., 2012NICHOLSON, K.E., CROTHER, B.I., GUYER, C. and SAVAGE, J.M., 2012. It is time for a new classification of anoles (Squamata: dactyloidae). Zootaxa, vol. 108, no. 1, pp. 1-108. http://dx.doi.org/10.11646/zootaxa.3477.1.1.
http://dx.doi.org/10.11646/zootaxa.3477....
), is supported by three major groups and represented by 175 species. Of these, 150 belong to the group N. auratus (Daudin, 1802), including N. fuscoauratus, which is an anole with greater distribution in South America that lives in areas of primary and secondary forests as well as forest edges (Vitt et al., 2003VITT, L.J., AVILA-PIRES, T.C.S., ZANI, P.A., SARTORIUS, S.S. and ESPÓSITO, M.C., 2003. Life above ground: ecology of Anolis fuscoauratus in the Amazon rain forest, and comparisons with its nearest relatives. Canadian Journal of Zoology, vol. 81, no. 1, pp. 142-156. http://dx.doi.org/10.1139/z02-230.
http://dx.doi.org/10.1139/z02-230...
). Their wide distribution allows them to enjoy a least concern conservation status and makes it a good object of study because, despite this privilege, ecological aspects of the Atlantic Forest populations are unknown, since there is a concentration of information restricted to the Amazon Forest (e.g., Bursey et al., 2005BURSEY, C.R., GOLDBERG, S.R. and PARMELEE, J.R., 2005. Gastrointestinal helminths from 13 species of lizards from Reserva Cuzco Amazonico, Peru. Comparative Parasitology, vol. 72, no. 1, pp. 50-68. http://dx.doi.org/10.1654/4132.
http://dx.doi.org/10.1654/4132...
; Goldberg et al., 2006aGOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006a. Helminths of the Brown-eared anole, Norops fuscoauratus (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Phyllomedusa, vol. 5, no. 1, pp. 83-86. http://dx.doi.org/10.11606/issn.2316-9079.v5i1p83-86.
http://dx.doi.org/10.11606/issn.2316-907...
). In this study we investigated the composition of macro endoparasites associated with N. fuscoauratus in the Atlantic Forest on the northeast of Brazil and indicated the infection rates and their relations with seasonality, sex and size of the host.

2. Material and Methods

2.1. Data collection

The lizards were collected by active search (manually), pitfall traps (196 buckets arranged in 49 sets), and glue traps (100 adhesives distributed per campaign) in Atlantic Forest fragments located in Centro de Instrução Marechal Newton Cavalcanti (CIMNC) (7°49’54” S, 35°6’10” W), in Pernambuco, Brazil, between August 2014 and July 2015, with a total of twelve excursions; and in Mata da Bananeira, Ecological Station of Murici (ESEC de Murici) (9°12’47” S, 35°52’9” W), Alagoas, Brazil, between December 2012 and June 2015, with eighteen excursions. The forest fragment in Pernambuco is composed of secondary vegetation of tropical rain forest and semi deciduous forest, with elevation between 50 and 100 m. In Alagoas the fragment is composed of primary vegetation of dense forest, open and seasonal forest, with elevation between 200 and 640 m. The N. fuscoauratus collected were euthanized with lidocaine hydrochloride 2%, weighed by a scale type Pesola ® and had recorded with the aid of a digital callipers, measures snout-vent length (SVL), later had their body cavities analyzed in search of parasites, which occurred on a stereomicroscope, which when found form preserved in 70% ethanol. After dissection, the lizards were fixed in 10% formalin and preserved in 70% alcohol. All parasites found were mounted on slides with the aid of lactophenol and analyzed under light microscope.

2.2. Statistical analysis

Infection rates (prevalence, mean intensity and probably ranges) were calculated according to Bush et al. (1997)BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. and SHOSTAKI, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, vol. 83, no. 4, pp. 575-583. http://dx.doi.org/10.2307/3284227.
http://dx.doi.org/10.2307/3284227...
and the discrepancy index (D) was calculated according Poulin (1993)POULIN, R., 1993. The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology, vol. 23, no. 7, pp. 937-944. http://dx.doi.org/10.1016/0020-7519(93)90060-C. PMid:8106186.
http://dx.doi.org/10.1016/0020-7519(93)9...
. This index is the minimum value of 0 (D=0) when all hosts have the same number of parasites and a maximum value of 1 (D=1) when all the parasites are aggregated into a single host. The index was calculated using the Quantitative Parasitology 3.0 (Rózsa et al., 2000RÓZSA, L., REICZIGEL, J. and MAJOROS, G., 2000. Quantifying parasites in samples of hosts. The Journal of Parasitology, vol. 86, no. 2, pp. 228-232. http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2. PMid:10780537.
http://dx.doi.org/10.1645/0022-3395(2000...
). A simple linear regression was performed to verify the relationship between the abundance of parasites and the size (SVL) of the host (Zar, 1999ZAR, J.H., 1999. Biostatistical analysis. New Jersey: Prentice Hall, 663 p.). To investigate the existence of seasonal variation in the abundance of endoparasites in N. fuscoauratus between the sexes and the interaction between seasonality and sexes we used a Generalized Linear Model (GLM) assuming a Poisson distribution. To conduct all analyses, we used only the adult hosts aiming to avoid the influence of ontogenetic factors. Were also excluded data flatworm larvae. The software used for analysis was Statistica version 8.0. For all tests, the significance level was 5%. Voucher specimens of hosts were deposited in the Coleção Herpetológica da Universidade Federal do Pernambuco (CHUFPE), and Coleção Herpetológica do Museu de História Natural da Universidade Federal de Alagoas (MHN-UFAL), and parasites in the Coleção de Parasitas do Laboratório de Biologia e Ecologia de Animais Silvestres (LABEAS), Universidade Federal do Cariri- UFCA (CHERP-P-UFCA).

2.3. Ethical approval

We authors state that our research has followed all ethical and policy regulations on the use of animals with proper authorizations and permits of national organs. The collecting methods were defined and authorized by regulamentory agency in Brazil (ICMBio/SISBio: 33507-1, 43750-1, and 43750-2). The research related to animal’s use has been complied with all the relevant national regulations and institutional policies for the care and use of animals.

3. Results

We examined 74 specimens of Norops fuscoauratus: 33 adult males (SVL= 38.8 ± 6.3 mm, weight= 1.0 ± 0.3 g), 33 adult females (SVL= 41.2 ± 7.1 mm; weight= 1.5 ± 0.6 g), and 8 juveniles (SVL= 28.5 ± 3.8 mm, weight= 0.4 ± 0.1 g). Overall the prevalence of endoparasites was 35.1% (26/74), being 53.9% adult females, 34.6% adult males, and 11.5% juveniles. Five species of helminths were reported to the lizard N. fuscoauratus (Table 1).

Table 1
Review of helminth fauna associated to Norops fuscoauratus indicating prevalence rates P (%) and mean intensity of infection (MI) versus the respective sites of infection (SI).

The abundance of macro endoparasites analysed was higher in the population of N. fuscoauratus of Pernambuco (N= 48) compared to the Alagoas (N= 26). In the first, we find five categories of helminths: Cystacanth (D= 0.768; range= 1-4), Larva of flatworm (D= 1), Physaloptera retusa (D= 0.95, range= 3-60), Rhabdias sp. (D= 1) and Strongyluris oscari (D= 1). Already in anoles of Murici (AL), we obtained two species of nematodes associated with the population of N. fuscoauratus: Rhabdias sp. (D= 1) and Strongyluris oscari (D= 0.84; range= 1-3). In general, the sex of the lizards influenced the abundance of endoparasites (Table 2), with more females than males being infested with parasites.

Table 2
Result of the GLM analysis, for the relationship between helminth abundance, and the collection period (dry vs. rainy), helminth abundance versus sex, and sex versus collection period of Norops fuscoauratus in the Atlantic Forest, northeastern Brazil.

The collection period, by itself, did not influence the abundance of parasites, but when associated with the sex of the lizards, there was a positive relationship with the abundance of helminths, with more females than males being infested with parasites during the rainy season. For both populations the intensity of infection was not correlated with the size (SVL) of the host (F= (1.22) 0.1545, P <0.69).

4. Discussion

Norops fuscoauratus is appointed for second time intermediate host of Acanthocephala in Cystacanth phase (Santos Mesquita et al., 2020SANTOS MESQUITA, J.M., OLIVEIRA, S.S., PEREZ, R. and ÁVILA, R.W., 2020. Helminths associated with Norops fuscoauratus (Squamata, Dactyloidae) in highland marshes of the Brazilian semi-arid. Journal of Helminthology, vol. 94, no. e153, pp. 1-7. http://dx.doi.org/10.1017/S0022149X20000358. PMid:32390581.
http://dx.doi.org/10.1017/S0022149X20000...
). In this study, these parasites were found in the body cavity and gastrointestinal organs and confirm the relationship between the site of infection in the host and the way of transmission of endoparasites. Acanthocephala phylum comprises generalists parasites which infect insectivores (e.g., lizards and frogs), in different environments, suggesting a life story without extensive restrictions to the intermediate host and the site of infection (Yamaguti, 1963YAMAGUTI, S., 1963. Systema helminthum. V. Acanthocephala. New York: Interscience Publishers, 860 p.; Ribas et al., 1995RIBAS, S.C., ROCHA, C.F.D., TEIXEIRA-FILHO, P.F. and VICENTE, J.J., 1995. Helminths (Nematoda) of the lizard Cnemidophorus ocellifer (Sauria: Teiidae): Assessing the effect of rainfall, body size and sex in the nematode infection rates. Ciencia e Cultura, vol. 47, pp. 88-91.; Goldberg et al., 2014GOLDBERG, S.R., BURSEY, C.R. and ARREOLA, J., 2014. Gastrointestinal Helminths of the Santa Cruz Island Sator, Sceloporus angustus (Squamata : Phrynosomatidae), from Isla Santa Cruz, Baja California Sur, Mexico. Comparative Parasitology, vol. 81, no. 2, pp. 276-277. http://dx.doi.org/10.1654/4676.1.
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). Representatives of this group of parasites were recorded infecting anoles from N. auratus group as N. sagrei (Duméril and Bibron, 1837) (Goldberg and Bursey, 2000GOLDBERG, S.R. and BURSEY, C.R., 2000. Transport of helminths to Hawaii via the brown anole, Anolis sagrei (Polychrotidae). The Journal of Parasitology, vol. 86, no. 4, pp. 750-755. http://dx.doi.org/10.1645/0022-3395(2000)086[0750:TOHTHV]2.0.CO;2. PMid:10958451.
http://dx.doi.org/10.1645/0022-3395(2000...
), N. limifrons (Cope, 1862) (Bursey and Goldberg, 2003BURSEY, C.R. and GOLDBERG, S.R., 2003. Acanthocephalus saurius n. sp. (Acanthocephala: Echinorhynchidae) and other helminths from the lizard Norops limifrons (Sauria: Polychrotidae) from Costa Rica. The Journal of Parasitology, vol. 89, no. 3, pp. 573-576. http://dx.doi.org/10.1645/GE-3120. PMid:12880258.
http://dx.doi.org/10.1645/GE-3120...
), N. uniformis (Cope, 1885) (Cabrera-Guzman and Garrido-Olvera, 2014), N. chrysolepis (Duméril and Bibron, 1837) (N. nitens) (Goldberg et al., 2010GOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2010. Helminths of Anolis nitens (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Herpetological Bulletin, vol. 112, pp. 903-912.), N. capito (Peters, 1863), N. humilis (Peters, 1863), and N. pachypus (Cope, 1875), presenting the latter, their prevalence rates: 15.2%, 5.7% and 14.3% (Bursey et al., 2012BURSEY, C.R., GOLDBERG, S.R., TELFORD JUNIOR, S.R. and VITT, L.J., 2012. Metazoan endoparasites of 13 species of Central American anoles (Sauria: Polychrotidae: Anolis) with a review of the helminth communities of Caribbean, Mexican, North American, and South American anoles. Comparative Parasitology, vol. 79, no. 1, pp. 75-132. http://dx.doi.org/10.1654/4530.1.
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), to another group of the same genus, as N. lineatopus (Gray, 1840) (Vogel and Bundy, 1987VOGEL, P. and BUNDY, D.A.P., 1987. Helminth parasites of Jamaican anoles (Reptilia: Iguanidae): Variation in prevalence and intensity with host age and sex in a population of Anolis lineatopus. Parasitology, vol. 94, no. 2, pp. 399-404. http://dx.doi.org/10.1017/S0031182000054044.
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). Once infected, lizards become paratenic to be preyed upon by a definitive host (e.g., birds and mammals) (Anderson, 2000ANDERSON, R.C., 2000. Nematode parasites of vertebrates: their development and transmission. 2nd ed. New York: CABI Internacional, 650 p. http://dx.doi.org/10.1079/9780851994215.0000.
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). The high prevalence rate of cystacanths (37.5%), the largest ever recorded for anoles lizards, in N. fuscoauratus collected in the Atlantic Forest of the state of Pernambuco and the absence of these helminths in lizards collected in the state of Alagoas, suggest that the environment should influence the level of infection of the parasite, and the Atlantic Forest region of CIMNC (PE) more inclined to the spread of the identified acanthocephalan.

Physaloptera retusa (Nematoda: Physalopteridae), one helminth using lizards as one of their hosts, it was found strongly adhered to the internal tissue of the stomach. This intense connection with the mucosal surface epithelium cause injuries and even total loss of gastric glands in the anchoring region, which may hinder the host digestion capacity (Goldberg and Bursey, 1989GOLDBERG, S.R. and BURSEY, C.R., 1989. Physaloptera retusa (Nematoda, Physalopteridae) in naturally infected sagebrush lizards, Sceloporus graciosus (Iguanidae). Journal of Wildlife Diseases, vol. 25, no. 3, pp. 425-429. http://dx.doi.org/10.7589/0090-3558-25.3.425. PMid:2761018.
http://dx.doi.org/10.7589/0090-3558-25.3...
). We thus evidenced the importance of these organisms in the population dynamics, therefore, to complete their life cycles, parasites can act affecting behaviour, intraspecific relations and various other aspects of the biology of the hosts (Marcogliese, 2004MARCOGLIESE, D.J., 2004. Parasites: small players with crucial roles in the ecological theater. EcoHealth, vol. 1, no. 2, pp. 151-164. http://dx.doi.org/10.1007/s10393-004-0028-3.
http://dx.doi.org/10.1007/s10393-004-002...
). In the N. auratus group, this nematode had already been reported to Norops nitens (McAllister et al., 2010MCALLISTER, C.T., BURSEY, C.R. and FREED, P., 2010. Helminth parasites of herpetofauna from the Rupunini District, Southwestern Guyana. Comparative Parasitology, vol. 77, no. 2, pp. 184-201. http://dx.doi.org/10.1654/4420.1.
http://dx.doi.org/10.1654/4420.1...
), N. lionotus (Cope, 1861), N. humilis and N. cupreus (Hallowell, 1860) (Bursey and Brooks, 2010BURSEY, C.R. and BROOKS, D.R., 2010. Nematode parasites of 16 lizard species from the Area de Conservación Guanacaste, Costa Rica. Comparative Parasitology, vol. 77, no. 2, pp. 232-235. http://dx.doi.org/10.1654/4429.1.
http://dx.doi.org/10.1654/4429.1...
), N. biporcatus (Wiegmann, 1834) and N. capito with prevalence of 2.3% and 6.1% for the last two, respectively (Bursey et al., 2012BURSEY, C.R., GOLDBERG, S.R., TELFORD JUNIOR, S.R. and VITT, L.J., 2012. Metazoan endoparasites of 13 species of Central American anoles (Sauria: Polychrotidae: Anolis) with a review of the helminth communities of Caribbean, Mexican, North American, and South American anoles. Comparative Parasitology, vol. 79, no. 1, pp. 75-132. http://dx.doi.org/10.1654/4530.1.
http://dx.doi.org/10.1654/4530.1...
) and N. brasiliensis (Vanzolini and Williams, 1970; Amorim and Ávila, 2019AMORIM, D.M. and ÁVILA, R.W., 2019. Infection patterns of helminths in Norops Brasiliensis (Squamata, Dactyloidae) from a Humid Forest, Northeastern Brazil and their relation with body mass, sex, host size, and season. Helminthologia, vol. 56, no. 2, pp. 168-174. http://dx.doi.org/10.2478/helm-2019-0011. PMid:31662688.
http://dx.doi.org/10.2478/helm-2019-0011...
). Relative to N. fuscoauratus, three studies were carried out reporting the occurrence of this species in the digestive tract. Goldberg et al. (2006a)GOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006a. Helminths of the Brown-eared anole, Norops fuscoauratus (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Phyllomedusa, vol. 5, no. 1, pp. 83-86. http://dx.doi.org/10.11606/issn.2316-9079.v5i1p83-86.
http://dx.doi.org/10.11606/issn.2316-907...
observed a prevalence rate of 1.8% for P. retusa, while this study identified the value of 4.16% (Table 1). Avila and Silva (2013) and Albuquerque et al. (2012)ALBUQUERQUE, S., ÁVILA, R.W. and BERNARDE, P.S., 2012. Occurrence of Helminths in Lizards (Reptilia: Squamata) at Lower Moa River Forest, Cruzeiro do Sul, Acre, Brazil. Comparative Parasitology, vol. 79, no. 1, pp. 64-67. http://dx.doi.org/10.1654/4539.1.
http://dx.doi.org/10.1654/4539.1...
did not provide data on infection rates for comparison, but the present study was similar as to the sites of infection, such as intestine and especially stomach.

Strongyluris oscari (Nematoda: Heterakidae), despite being one of the few representatives for the genus in Brazil, is an endoparasite associated with lizards in different ecosystems of the country (Ávila et al., 2011ÁVILA, R.W., CARDOSO, M.W., ODA, F.H. and SILVA, R.J., 2011. Helminths from Lizards (Reptilia: Squamata) at the Cerrado of Goiás State, Brazil. Comparative Parasitology, vol. 78, no. 1, pp. 120-128. http://dx.doi.org/10.1654/4472.1.
http://dx.doi.org/10.1654/4472.1...
, 2012ÁVILA, R.W., ANJOS, L.A., RIBEIRO, S.C., MORAIS, D.H., SILVA, R.J. and ALMEIDA, W.O., 2012. Nematodes of Lizards (Reptilia : Squamata) from Caatinga biome, Northeastern Brazil. Comparative Parasitology, vol. 79, no. 1, pp. 56-63. http://dx.doi.org/10.1654/4518.1.
http://dx.doi.org/10.1654/4518.1...
; Barreto-Lima and Anjos, 2014BARRETO-LIMA, A.F. and ANJOS, L.A., 2014. Occurrence of Strongyluris oscari (Nematoda; Heterakidae) in Enyalius bilineatus (Squamata: Leiosaurinae) from the Brazilian Atlantic Forest. Herpetology Notes, vol. 7, pp. 455-456.; Cabral et al., 2018CABRAL, A.N., TELES, D.A., BRITO, S.V., ALMEIDA, W.O., ANJOS, L.A., GUARNIERI, M.C. and RIBEIRO, S.C., 2018. Helminth parasites of Mabuya arajara Rebouças-Spieker, 1981 (Lacertilia: Mabuyidae) from Chapada do Araripe, northeastern Brazil. Parasitology Research, vol. 117, no. 4, pp. 1185-1193. http://dx.doi.org/10.1007/s00436-018-5797-7. PMid:29435716.
http://dx.doi.org/10.1007/s00436-018-579...
). Their occurrence has been cited previously in anoles (Goldberg et al., 2006bGOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006b. Parasites of two lizard species, Anolis punctatus and Anolis transversalis (Squamata: Polychrotidae) from Brazil and Ecuador. Amphibia-Reptilia, vol. 27, no. 4, pp. 575-579. http://dx.doi.org/10.1163/156853806778877068.
http://dx.doi.org/10.1163/15685380677887...
). To N. fuscoauratus of the Amazon Forest, this nematode is also a relatively common parasitic association (Ávila and Silva, 2010ÁVILA, R.W. and SILVA, R.J., 2010. Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. The Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 16, no. 4, pp. 543-572. http://dx.doi.org/10.1590/S1678-91992010000400005.
http://dx.doi.org/10.1590/S1678-91992010...
, 2013ÁVILA, R.W. and SILVA, R.J., 2013. Helminths of lizards from the municipality of Aripuanã in the southern Amazon region of Brazil. Journal of Helminthology, vol. 87, no. 1, pp. 12-16. http://dx.doi.org/10.1017/S0022149X11000769. PMid:22166366.
http://dx.doi.org/10.1017/S0022149X11000...
) and reached different prevalence rates, such that the presented in Bursey et al. (2005)BURSEY, C.R., GOLDBERG, S.R. and PARMELEE, J.R., 2005. Gastrointestinal helminths from 13 species of lizards from Reserva Cuzco Amazonico, Peru. Comparative Parasitology, vol. 72, no. 1, pp. 50-68. http://dx.doi.org/10.1654/4132.
http://dx.doi.org/10.1654/4132...
(4%) and Goldberg et al. (2006a)GOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006a. Helminths of the Brown-eared anole, Norops fuscoauratus (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Phyllomedusa, vol. 5, no. 1, pp. 83-86. http://dx.doi.org/10.11606/issn.2316-9079.v5i1p83-86.
http://dx.doi.org/10.11606/issn.2316-907...
(28.6% and 38%, respectively). Teixeira et al. (2020)TEIXEIRA, A.A.M., RIUL, P., BRITO, S.V., ARAUJO-FILHO, J.A., TELES, D.A., ALMEIDA, W.O. and MESQUITA, D.O., 2020. Ecological release in lizard endoparasites from the Atlantic Forest, northeast of the Neotropical Region. Parasitology, vol. 147, no. 4, pp. 491-450. http://dx.doi.org/10.1017/S0031182020000025. PMid:31965954.
http://dx.doi.org/10.1017/S0031182020000...
also register this parasite in the Atlantic Forest of Northeast Brazil with a 50% prevalence (N=7). Its occurrence in the two populations of N. fuscoauratus in this study only confirms the extent of the parasite-host relationship, which was more evident in lizards from Murici (AL) (P=17.85%) compared to the CIMNC (PE) (P=2.08%).

Anderson (2000)ANDERSON, R.C., 2000. Nematode parasites of vertebrates: their development and transmission. 2nd ed. New York: CABI Internacional, 650 p. http://dx.doi.org/10.1079/9780851994215.0000.
http://dx.doi.org/10.1079/9780851994215....
supports that abiotic factors in general interfere in the development and act as the main responsible factor for the type of infection caused by parasites, especially when we talk about Rhabdias spp. (Nematoda: Rhabdiasidae) that alternate between the free and parasite life cycles. Nematodes of this genus, different from the diet-spinoff helminths (heteroxenous) were detected in the respiratory tract of N. fuscoauratus, the default location for these worms when compared with studies conducted for other hosts (Tkach et al., 2014TKACH, V.V., KUZMIN, Y. and SNYDER, S.D., 2014. Molecular insight into systematics, host associations, life cycles and geographic distribution of the nematode family Rhabdiasidae. International Journal for Parasitology, vol. 44, no. 5, pp. 273-284. http://dx.doi.org/10.1016/j.ijpara.2013.12.005. PMid:24560917.
http://dx.doi.org/10.1016/j.ijpara.2013....
). Rhabdias spp. are usually reported parasitizing lizards, particularly the anoles as well represented by Torres-Ortiz (1980)TORRES-ORTIZ, R.A., 1980. Otro hospedador final para Rhabdias sp. (Nematoda) e implicaciones evolutivas de las especies del hospedador. Caribbean Journal of Science, vol. 16, pp. 109-114., Bundy et al. (1987)BUNDY, D.A.P., VOGEL, P. and HARRIS, E.A., 1987. Helminth parasites of Jamaican Anoles (Reptilia: Iguanidae): a comparison of the helminth fauna of 6 Anolis species. Journal of Helminthology, vol. 61, no. 1, pp. 77-83. http://dx.doi.org/10.1017/S0022149X00009767.
http://dx.doi.org/10.1017/S0022149X00009...
, Dobson et al. (1992)DOBSON, A.P., PACALA, S.V., ROUGHGARDEN, J.D., CARPER, E.R. and HARRIS, E.A., 1992. The parasites of Anolis lizards in the northern Lesser Antilles I. Patterns of distribution and abundance. Oecologia, vol. 91, no. 1, pp. 110-117. http://dx.doi.org/10.1007/BF00317248. PMid:28313381.
http://dx.doi.org/10.1007/BF00317248...
, Bursey et al. (2003BURSEY, C.R., GOLDBERG, S.R. and TELFORD JUNIOR, S.R., 2003. Rhabdias anolis n. sp. (Nematoda: Rhabdiasidae) from a lizard, Anolis frenatus (Sauria: Polychrotidae), from Panama. The Journal of Parasitology, vol. 89, no. 1, pp. 113-117. http://dx.doi.org/10.1645/0022-3395(2003)089[0113:RANSNR]2.0.CO;2. PMid:12659312.
http://dx.doi.org/10.1645/0022-3395(2003...
, 2005)BURSEY, C.R., GOLDBERG, S.R. and PARMELEE, J.R., 2005. Gastrointestinal helminths from 13 species of lizards from Reserva Cuzco Amazonico, Peru. Comparative Parasitology, vol. 72, no. 1, pp. 50-68. http://dx.doi.org/10.1654/4132.
http://dx.doi.org/10.1654/4132...
, Goldberg et al. (2006bGOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006b. Parasites of two lizard species, Anolis punctatus and Anolis transversalis (Squamata: Polychrotidae) from Brazil and Ecuador. Amphibia-Reptilia, vol. 27, no. 4, pp. 575-579. http://dx.doi.org/10.1163/156853806778877068.
http://dx.doi.org/10.1163/15685380677887...
, 2010)GOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2010. Helminths of Anolis nitens (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Herpetological Bulletin, vol. 112, pp. 903-912., Vrcibradic et al. (2007VRCIBRADIC, D., VICENTE, J.J. and BURSEY, C.R., 2007. Helminths infecting the lizard Enyalius bilineatus (Iguanidae, Leiosaurinae), from an Atlantic Rainforest area in Espirito Santo state, southeastern Brazil. Amphibia-Reptilia, vol. 28, no. 1, pp. 166-169. http://dx.doi.org/10.1163/156853807779799009.
http://dx.doi.org/10.1163/15685380777979...
, 2008)VRCIBRADIC, D., ANJOS, L.A., VICENTE, J.J. and BURSEY, C.R., 2008. Helminth parasites of two sympatric lizards, Enyalius iheringii and E. perditus (Leiosauridae), from an Atlantic Rainforest area of southeastern Brazil. Acta Parasitologica, vol. 53, no. 2, pp. 222-225. http://dx.doi.org/10.2478/s11686-008-0027-6.
http://dx.doi.org/10.2478/s11686-008-002...
, Ávila et al. (2011)ÁVILA, R.W., CARDOSO, M.W., ODA, F.H. and SILVA, R.J., 2011. Helminths from Lizards (Reptilia: Squamata) at the Cerrado of Goiás State, Brazil. Comparative Parasitology, vol. 78, no. 1, pp. 120-128. http://dx.doi.org/10.1654/4472.1.
http://dx.doi.org/10.1654/4472.1...
and Ribeiro et al. (2012)RIBEIRO, S.C., FERREIRA, F.S., BRITO, S.V., TELES, D.A., ÁVILA, R.W., ALMEIDA, W.O., ANJOS, L.A. and GUARNIERI, M.C., 2012. Pulmonary infection in two sympatric lizards, Mabuya arajara (Scincidae) and Anolis brasiliensis (Polychrotidae) from a cloud forest in Chapada do Araripe, Ceará, Northeastern Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 4, pp. 929-933. http://dx.doi.org/10.1590/S1519-69842012000500021. PMid:23295524.
http://dx.doi.org/10.1590/S1519-69842012...
. For N. fuscoauratus, these helminths are relatively common, and associations have been discovered in two stages: in the first, a prevalence rate of 1.8% was expressed (Goldberg et al., 2006aGOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006a. Helminths of the Brown-eared anole, Norops fuscoauratus (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Phyllomedusa, vol. 5, no. 1, pp. 83-86. http://dx.doi.org/10.11606/issn.2316-9079.v5i1p83-86.
http://dx.doi.org/10.11606/issn.2316-907...
) - similar to the rates obtained for the analysed population in this study (PE=2.08% and AL=3.57%) - and the second time, were located both inhabiting the lung and the stomach of lizards (Avila and Silva, 2010). Recently, Santos Mesquita et al. (2020)SANTOS MESQUITA, J.M., OLIVEIRA, S.S., PEREZ, R. and ÁVILA, R.W., 2020. Helminths associated with Norops fuscoauratus (Squamata, Dactyloidae) in highland marshes of the Brazilian semi-arid. Journal of Helminthology, vol. 94, no. e153, pp. 1-7. http://dx.doi.org/10.1017/S0022149X20000358. PMid:32390581.
http://dx.doi.org/10.1017/S0022149X20000...
also registered these parasites, with slightly higher prevalence (8%).

The larvae of monogenic flatworms are reported for the first time infecting N. fuscoauratus because, until then, only Ophiotaenia sp. (Platyhelminthes: Cestoda) and Urotrema shirleyae Zamparo, Brooks and Tkach, 2005 (Platyhelminthes: Digenea) were identified parasitizing this species of lizard (Goldberg et al., 2006aGOLDBERG, S.R., BURSEY, C.R. and VITT, L.J., 2006a. Helminths of the Brown-eared anole, Norops fuscoauratus (Squamata, Polychrotidae), from Brazil and Ecuador, South America. Phyllomedusa, vol. 5, no. 1, pp. 83-86. http://dx.doi.org/10.11606/issn.2316-9079.v5i1p83-86.
http://dx.doi.org/10.11606/issn.2316-907...
; Avila and Silva, 2010). The site of infection (digestive tract) for these helminths also suggests contamination acquired by food.

In specific studies, size, sex, and age of the lizards tend to influence prevalence rates, amplitude and mean intensity of infection (Anjos et al., 2005ANJOS, L.A., ROCHA, C.F.D., VRCIBRADIC, D. and VICENTE, J.J., 2005. Helminths of the exotic lizard Hemidactylus mabouia from a rock outcrop area in southeastern Brazil. Journal of Helminthology, vol. 79, no. 4, pp. 307-313. http://dx.doi.org/10.1079/JOH2005288. PMid:16336713.
http://dx.doi.org/10.1079/JOH2005288...
; Amorim and Ávila, 2019AMORIM, D.M. and ÁVILA, R.W., 2019. Infection patterns of helminths in Norops Brasiliensis (Squamata, Dactyloidae) from a Humid Forest, Northeastern Brazil and their relation with body mass, sex, host size, and season. Helminthologia, vol. 56, no. 2, pp. 168-174. http://dx.doi.org/10.2478/helm-2019-0011. PMid:31662688.
http://dx.doi.org/10.2478/helm-2019-0011...
). In Enyalius perditus Jackson, 1978, for example, greater host and therefore older showed the highest rates evaluated and the males of the species, which were more parasitized than females (Sousa et al., 2007SOUSA, B.M., LIMA, S.S. and OLIVEIRA, A., 2007. Gastrointestinal helminth fauna of Enyalius perditus (Reptilia: Leiosauridae): Relation to host age and sex. The Journal of Parasitology, vol. 93, no. 1, pp. 211-213. http://dx.doi.org/10.1645/GE-852R1.1. PMid:17436969.
http://dx.doi.org/10.1645/GE-852R1.1...
). Although Vogel and Bundy (1987)VOGEL, P. and BUNDY, D.A.P., 1987. Helminth parasites of Jamaican anoles (Reptilia: Iguanidae): Variation in prevalence and intensity with host age and sex in a population of Anolis lineatopus. Parasitology, vol. 94, no. 2, pp. 399-404. http://dx.doi.org/10.1017/S0031182000054044.
http://dx.doi.org/10.1017/S0031182000054...
have obtained the same result for N. lineatopus – males more parasitized than females - the inverse was seen in this study: in general, the endoparasites found were more abundant in females than in males of N. fuscoauratus. Amorim and Ávila (2019)AMORIM, D.M. and ÁVILA, R.W., 2019. Infection patterns of helminths in Norops Brasiliensis (Squamata, Dactyloidae) from a Humid Forest, Northeastern Brazil and their relation with body mass, sex, host size, and season. Helminthologia, vol. 56, no. 2, pp. 168-174. http://dx.doi.org/10.2478/helm-2019-0011. PMid:31662688.
http://dx.doi.org/10.2478/helm-2019-0011...
studying N. brasiliensis did not obtain in their study significant relationship between abundance of the trematode Mesocoelium monas (Rudolphi, 1819) and host sex or season, although the abundance of this parasite increased significantly with host body size and mass, while abundance of nematodes was related to season and host mass.

The difference in the abundance of parasites between the sexes and between collection period related to the sexes is due to intrinsic ecological and physiological factors (Aho, 1990AHO, J.M., 1990. Helminthes communities of amphibians and reptiles: comparative approaches to understanding patterns and process. In: G. W. ESCH, A. O. BUSH and J. M. AHO, eds. Parasite communities: patterns and process. Netherlands: Springer, pp. 157-190. http://dx.doi.org/10.1007/978-94-009-0837-6_7.
http://dx.doi.org/10.1007/978-94-009-083...
) and/or, especially, sexual dimorphism, because studies show the relationship positive between body size and parasitic infection rates (Ribas et al., 1995RIBAS, S.C., ROCHA, C.F.D., TEIXEIRA-FILHO, P.F. and VICENTE, J.J., 1995. Helminths (Nematoda) of the lizard Cnemidophorus ocellifer (Sauria: Teiidae): Assessing the effect of rainfall, body size and sex in the nematode infection rates. Ciencia e Cultura, vol. 47, pp. 88-91.; Sousa et al., 2007SOUSA, B.M., LIMA, S.S. and OLIVEIRA, A., 2007. Gastrointestinal helminth fauna of Enyalius perditus (Reptilia: Leiosauridae): Relation to host age and sex. The Journal of Parasitology, vol. 93, no. 1, pp. 211-213. http://dx.doi.org/10.1645/GE-852R1.1. PMid:17436969.
http://dx.doi.org/10.1645/GE-852R1.1...
). It is known that the females of N. fuscoauratus are significantly larger than males on the snout-vent length (SVL) and the width of the body (Vitt et al., 2003VITT, L.J., AVILA-PIRES, T.C.S., ZANI, P.A., SARTORIUS, S.S. and ESPÓSITO, M.C., 2003. Life above ground: ecology of Anolis fuscoauratus in the Amazon rain forest, and comparisons with its nearest relatives. Canadian Journal of Zoology, vol. 81, no. 1, pp. 142-156. http://dx.doi.org/10.1139/z02-230.
http://dx.doi.org/10.1139/z02-230...
; and unpublished data) so it is consistent to suggest that sexual dimorphism in relation to body size may cause such differences in the incidence of parasites.

Although there is a smaller range of associated endoparasites, the N. fuscoauratus from Murici (AL) had a greater range of the nematodes Rhabdias sp. and S. oscari compared to the CIMNC (PE) and a highly added Poulin discrepancy index (D=0.84) for the latter parasite. Based on the claim submitted by Poulin (1993)POULIN, R., 1993. The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology, vol. 23, no. 7, pp. 937-944. http://dx.doi.org/10.1016/0020-7519(93)90060-C. PMid:8106186.
http://dx.doi.org/10.1016/0020-7519(93)9...
, lower values in the prevalence rate accentuate the aggregation of parasites in the host, but this was not observed for the population of N. fuscoauratus from Alagoas, because it had a higher prevalence rate (17.85%) among the other hosts listed in Table 1. Probably this result was a reflection of the sample size difference between populations.

Poulin (2007)POULIN, R., 2007. Evolutionary ecology of parasites. 2nd ed. Princeton: Princeton University Press, 342 p. http://dx.doi.org/10.1515/9781400840809.
http://dx.doi.org/10.1515/9781400840809...
affirmed that the evolution of parasites takes into account the strategies developed for better success of their life cycles. The helminth categories identified in this study appear to conform more to the non-favouritism strategy because they are not specific to N. fuscoauratus and already notified to other host species in other areas surveyed. The differences in the diversity of macro endoparasites in two populations of N. fuscoauratus in the Atlantic Forest are attributed to individuals’ characteristics of environments occupied by animals, allowing slightly different diets and contacts with different species of helminths. Even though parasitological studies were previously developed for N. fuscoauratus, we contribute to the literature presenting new parasite associated with the species and increasing its geographical extent of activity, including the Atlantic Forest, a natural area with high biological diversity (Myers et al., 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B. and KENT, J., 2000. Biodiversity hotspots for conservation priorities. Nature, vol. 403, no. 6772, pp. 853-845. http://dx.doi.org/10.1038/35002501. PMid:10706275.
http://dx.doi.org/10.1038/35002501...
).

Acknowledgements

We are grateful to the Proof-Reading-Service.com Editorial Certification for suggestions and revision of the English version of the manuscript; Campo de Instrução Marechal Newton Cavalcante for their help with our field work; and Dra. Selma Torquato da Silva for the hospitality in the Museu de História Natural – Universidade Federal de Alagoas. We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES, and Pró-Reitoria de Pesquisa, Pós-Graduação e Inovação – PRPI (UFCA) for the research grant awarded to this study. We thank the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (BPI – FUNCAP: BP3-0139-00323.01.00/18; BP4-00172-00223.01.01/20).

References

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Publication Dates

  • Publication in this collection
    21 June 2021
  • Date of issue
    2022

History

  • Received
    03 Aug 2020
  • Accepted
    02 Dec 2020
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