First record of Sebekia oxycephala (Pentastomida: Sebekidae) infecting Helicops angulatus (Reptilia: Colubridae) in Northeast Brazil

Primeiro registro de Sebekia oxycephala (Pentastomida: Sebekidae) infectando Helicops angulatus (Reptilia: Colubridae) no Nordeste do Brasil

Abstract

In this study, we investigated the infection by pulmonary parasites in the water snake Helicops angulatus. We found four nymphs of the pentastomide parasite Sebekia oxycephala, parasitizing two adult females H. angulatus collected in the municipality of Rio Tinto, Paraíba, Brazil. This occurrence is likely due to the nymphs of this parasite directly infecting aquatic intermediate hosts, such as fish. The result of this study represents the first record of pentastomid infecting H. angulatus.

Keywords:
pentastomids; neotropical; parasite; snake

Resumo

Neste estudo investigamos a infecção por parasitos pulmonares na serpente Helicops angulatus. Encontramos quatro ninfas de pentastomídeos (Sebekia oxycephala) parasitando duas fêmeas adultas de H. angulatus oriundas do município de Rio Tinto, Paraíba, Brasil. A ocorrência das ninfas na serpente sugere que a transmissão ocorra através da cadeia trófica, uma vez que peixes atuam como hospedeiros intermediários do parasito e fazem parte da dieta H. angulatus . O resultado deste estudo representa o primeiro registro de pentastomídeos infectando H. angulatus.

Palavras-chave:
pentastomídeo; neotropical; parasito; serpente

1. Introduction

Pentastomids are a group of endoparasites that live in the respiratory tract of their hosts (Christoffersen and Assis, 2013). Currently, around 144 species of Pentastomida are registered and distributed in four orders: Eupentastomida, Porocephalida, Porocephaloidea, and Sebekidae (Lima et al., 2022). Some species of pentastomids are generalists (Almeida et al., 2009; Christoffersen and Assis, 2013), while others are specific hosts (Riley, 1986). Adult pentastomids are obligatory parasites found in the respiratory tract of reptiles such as snakes, lizards, crocodilians, and turtles in the tropical region (Christoffersen and Assis, 2013). On the other hand, larvae and nymphs of pentastomids are found infecting the respiratory tract of insects, amphibians, birds, fish, mammals, and even humans (Paré, 2008; Christoffersen and Assis, 2013, 2015a, b; Pavanelli et al., 2013). Sebekia Sambon, 1922 is a genus of pentastomids usually associated with crocodilians (Riley et al., 1990) distributed in the regions of Neotropical, Nearctic, Ethiopian, Australian, and Oriental (Riley et al., 1990) and species of the genus Sebekia use fishes as intermediate hosts (Almeida et al., 2010; Pavanelli et al., 2013; Cardoso et al., 2014). The genus Sebekia holds significant economic importance due to its ability to induce inflammatory reactions and hemorrhaging in cultured fish (Boyce et al., 1987).

Snakes can harbor a wide variety of parasites, acting as definitive, intermediate, and paratenic hosts (Castro et al., 2020; Oliveira et al., 2021; Ferreira-Silva et al., 2022), including aquatic snakes of the genus Helicops Wagler, 1830 (Rego and Vicente, 1988; Silva et al., 2015; Quirino et al., 2018). Helicops angulatus (Linnaeus, 1758) is a water snake, widely distributed in Brazil (Uetz et al., 2023). It primarily feeds on fish and amphibians (Santos-Costa et al., 2022) although records have shown the occurrence of lizards and earthworms in its diet (Strussmann et al., 2011; Teixeira et al., 2017).

Despite the widespread distribution of Helicops angulatus, our understanding of its endoparasitic fauna and the ecological parasite-host relationships remains limited. Here we report for the first time the occurrence of Sebekia oxycephala (Diesing, 1835) parasitizing H. angulatus.

2. Material and Methods

We analyzed two adult females of H. angulatus (Figure 1A). Both were collected during the years 2011 and 2013, under SISBIO collection permit No 22940-2, from the municipality of Rio Tinto (6°48'18.37”S, 35°4'26.75”W), state of Paraíba, Brazil. The snakes were euthanized with a lethal injection of 2% lidocaine hydrochloride. Snout-vent length (SVL) was measured with a precision caliper and weighed on a digital scale. Subsequently, they were fixed in 10% formaldehyde, preserved in 70% ethanol, and deposited in the Herpetology Collection of the Universidade Federal Paraíba (CHUFPB 364 and 947). Snakes were dissected under a stereoscopic for the verified of the presence of parasites in respiratory and gastrointestinal tracts. The endoparasites were counted and placed in glass vials containing 70% ethanol, and subsequently mounted on temporary slides for identification. Pentastomids were identified based on hook dimensions and body size (Almeida et al., 2010). Specimens were deposited in Parasitological Collection of the Regional University of Cariri (URCA P 1418, 1419, and 1420).

Figure 1
(A) Helicops angulatus from the municipality of Rio Tinto, Paraíba state, Brazil; (B) - nymph of Sekekia oxycephala parasite of H. angulatus.

3. Results and Discussion

The snakes were infected by four of the nymphs of the pentastomid Sebekia oxycephala (Figure 1B), with one snake having two nymphs in the stomach and one in the small intestine and the other snake having one nymph in the stomach.

Infection with Sebekia oxycephala may be related to the semiaquatic habit and piscivorous diet of this host, since the nymphs of Sebekia species use fishes with intermediate hosts (Junker et al., 1998; Almeida et al., 2010; Santos-Costa et al., 2022), suggesting the use of Helicops angulatus as a second intermediate host in the life cycle of this parasite. The Sebekia species has already been registered infecting other species of Helicops, such as H. leopardinus (Schlegel, 1837) in Pantanal, state of Mato Grosso (Rego & Vicente, 1988) and H. infrataeniatus (Jan, 1865) in the state de São Paulo (Silva et al., 2015). In addition, there are records of infection by Sebekia for other snakes such as Micrurus alleni Schmidt, 1936 (Goldberg and Bursey, 2004), M. surinamensis (Cuvier, 1816) (Ávila et al., 2013), Crotalus durissus Linnaeus, 1758 (Leidy, 1884), and Eunectes murinus (Linnaeus, 1758) (Lagunas-Calvo et al., 2020). According to the records in the literature, only two species of Sebekia (S. mississippiensis and S. oxycephala) parasitizing snakes are known (Table 1) (Lagunas-Calvo et al., 2020).

Table 1
Bibliographic review of Pentastomid species parasitizing snakes.

PENTASTOMIDA	HOST	LOCALITY	REFERENCES
Family Sebekidae Sambon, 1922
Sebekia mississippiensis (Overstreet, Self & Vilet, 1985)	Nerodia cyclopion (Duméril, Bibron & Duméril, 1854)	United States	Overstreet et al., (1985)
	Nerodia erythrogaster (Forster, 1771)	United States	Overstreet et al. (1985)
	Nerodia fasciata (Linnaeus, 1766)	United States	Overstreet et al. (1985)
	Nerodia rhombifer (Hallowell, 1852)	United States	Overstreet et al. (1985)
	Nerodia sipedon (Linnaeus, 1758)	United States	Overstreet et al., (1985)
	Nerodia taxispilota (Holbrook, 1838)	United States	Boyce et al. (1987)
Sebekia oxycephala (Diesing, 1835)	Helicops infrataeniatus (Jan, 1865)	Brazil	Silva et al. (2015)
	Micrurus surinamensis (Cuvier, 1816)	Brazil	Ávila et al. (2013)
	Crotalus durissus Linnaeus, 1758	United States	Leidy (1884)
	Eunectes murinus (Linnaeus, 1758)	United States	Lagunas-Calvo et al. (2020)
	Helicops angulatus (Linnaeus, 1758)	Brazil	Present study
Sebekia sp.	Helicops leopardinus (Schlegel, 1837)	Brazil	Rego and Vicente (1988)
	Micrurus alleni Schmidt, 1936	Costa Rica	Goldberg and Bursey (2004)

This is the first record of nymphs of S. oxycephala parasitizing H. angulatus. Little is known regarding the association of Sebekia spp. with snakes, as most published studies primarily focus on their association with definitive hosts. Consequently, there is a dearth of information regarding their ecology, life cycle, and the impact they have on their intermediate hosts. Hence, there is a crucial need research to enhance our understanding of these parasites and the potential consequences they inflict upon their intermediate hosts.

Acknowledgements

We thank Herivelto Oliveira for the photo of H. angulatus. MCO thanks the Fundação de Apoio à Pesquisa do Estado da Paraíba for fellowship. RLM thanks Paraíba State Research Foundation (FAPESQ) grant 006/2020 - PDCTR-PB 2020 and CNPQ 301852/2023-5; to o Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research grant to W. O. Almeida.

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Publication Dates

• Publication in this collection
  27 Nov 2023
• Date of issue
  2023

History

• Received
  01 June 2023
• Accepted
  23 Oct 2023