Eustrongylides uses piscivorous birds as definitive hosts, oligoquets as intermediate hosts and fish as second intermediate hosts. However, amphibians and reptiles can act as secondary or paratenic hosts. The following work presents the first record of Eustrongylides larvae in snakes in the Neotropics. The coelomic cavity of 101 snakes belonging to Helicops infrataeniatus, Philodryas aestiva, Philodryas olfersii, Philodryas patagoniensis, Erythrolamprus poecilogyrus, Erythrolamprus jaegeri, Atractus reticulatus, Dipsas ventrimaculatus, Thamnodynastes strigatus, Phalotris lemniscatus and Bothrops alternatus from southern Brazil were examined. Six H. infrataeniatus were parasitized with larvae of Eustrongylides sp. The encounter of these larvae only in this specie can be related to the aquatic habit of the snake, which allows ecological interactions with the definitive and intermediate hosts of the Eustrongylides cycle. The occurrence of these parasites in a Neotropical snake is registered for the first time, contributing to the knowledge of the helminth diversity associated to Brazilian snakes.Asociación Herpetológica Argentin

Mascarenhas, Carolina S.

Müller, Gertrud

Oliveira, Roger Jean

Veiga Pereira, Julia

Cuadernos de Herpetología

Servicio de Difusión de la Creación Intelectual

Nota151Author for correspondence: julia.veiga@outlook.comF i r s t  r e c o r d  o f  E u s t r o n g y l i d e s  s p.  ( N e m a t o d a : Dioctophymatidae) larvae parasitizing snakes in the Neotropical regionJulia Veiga Pereira¹, Roger Jean Oliveira², Carolina Silveira Mascarenhas², Gertrud Müller²¹Laboratório de Herpetologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Agronomia, CEP 91501-970, Porto Alegre, Rio Grande do Sul, Brazil.²Laboratório de Parasitologia de Animais Silvestres, Instituto de Biologia, Universidade Federal de Pelotas, Campus Universitário, CEP 96010-900, Pelotas, Rio Grande do Sul, Brazil.Cuad. herpetol. 35 (1): 151-155 (2021)Eustrongylides (Jägerskiöld, 1909) (Nematoda: Dioc-tophymatidae) was proposed for Dioctophymatidae species that cause tumors on the wall of the proven-triculus, mainly from piscivorous birds (Measures, 1988). Some species were reported in Gaviiformes, Podicipediformes, Pelecaniformes, Anseriformes, Charadriiformes, Ciconiiformes and Passeriformes (Measures, 1988). Eustrongylides consists of three species: Eustrongylides tubifex Jägerskiöld, 1909, Eu-strongylides ignotus (Jägerskiöld, 1909) and Eustron-gylides excisus (Jägerskiöld, 1909) (Melo et al., 2016).Regarding the geographical distribution of these parasites, Estrongylides ignotus has the widest distribution, occurring in the Nearctic, Neotropical and Australian regions. Eustrongylides excisus oc-curs in Europe and E. tubifex is present only in the Holartic and Neotropical regions (Measures, 1988).The life cycle of these parasites is not well known (Xiong et al., 2009), however, some studies indicate that these helminths use piscivorous birds as definitive hosts, oligoquets as intermediate hosts and usually fish as intermediate second hosts, with amphibians and reptiles as intermediate or paratenic hosts (Measure, 1988; Friend and Franson, 1999; Melo et al., 2016). Eustrongylides species may oc-casionally parasitize humans, thus demonstrating zoonotic potential (Xiong et al., 2009; Eiras et al., 2016).Little is known about the parasitism of Eu-strongylides species in wild snake populations, but larvae of these parasites have been reported in some Colubridae from North America, Europe and Asia, Recibida:  2 5  M a y o  2 0 2 0Revisada:  0 8  J u l i o  2 0 2 0Aceptada:  1 5  S e pt i e mbre  2 0 2 0Editor  Asociado:  C.  B or te irodoi:  10.31017/CdH.2020.(2020-042)ABSTRACTEustrongylides uses piscivorous birds as definitive hosts, oligoquets as intermediate hosts and fish as second intermediate hosts. However, amphibians and reptiles can act as secondary or paratenic hosts. The following work presents the first record of Eustrongylides larvae in snakes in the Neotropics. The coelomic cavity of 101 snakes belonging to Helicops infrataeniatus, Philodryas aestiva, Philodryas olfersii, Philodryas patagoniensis, Erythrolamprus poecilogyrus, Erythrolamprus jaegeri, Atractus reticulatus, Dipsas ventrimaculatus, Thamnodynastes strigatus, Phalotris lemniscatus and Bothrops alternatus from southern Brazil were examined. Six H. infra-taeniatus were parasitized with larvae of Eustrongylides sp. The encounter of these larvae only in this specie can be related to the aquatic habit of the snake, which allows ecological interactions with the definitive and intermediate hosts of the Eustrongylides cycle. The occurrence of these parasites in a Neotropical snake is registered for the first time, contributing to the knowledge of the helminth diversity associated to Brazilian snakes.Key Words: Helicops infrataeniatus; Helminths; Parasitism; Reptiles; Serpentes.152J. V. Pereira et al. - Eustrongylides sp. larvae in snakessuch as: Nerodia sipedon (Linnaeus, 1758), Natrix natrix (Linnaeus, 1751) and N. tessellata (Laurenti, 1768) (Bursey, 1986; Biserkov, 1995; Mihalca, 2007; Yildirimhan et al., 2007). In acrochordid snakes from Australia there are also reports of the occur-rence of these parasites (Jones, 1978). In captivity, larvae of Eustrongylides have been observed in some colubrid snakes such as Coluber constrictor (Lin-naeus, 1758), Masticophis flagellum (Shaw, 1802), Nerodia sipedon, Pituophis melanoleucus (Daudin, 1803), Thamnophis sirtalis (Linnaeus, 1758), as well as in the viperid snakes Bothrops atrox (Linnaeus, 1758) and Agkistrodon contortrix (Linnaeus, 1766) in North America (Winsor, 1948 in Bursey, 1986). In Brazil, while these nematodes have been reported in some hosts, such as birds (Vicente et al., 1995; Bernardon et al., 2017), amphibians (Melo et al., 2016) and fish (Isaac et al., 2004; Meneguetti et al., 2013; Carvalho et al., 2017), we know of no reports of their occurrence in snakes. The following work presents the first record of Eustrongylides larvae in wild snakes from the Neotropical region.One hundred and one specimens belonging to 11 species of snakes were examined: Helicops infrataeniatus Jan, 1865 (n=65), Philodryas aestiva (Duméril, Bibron & Duméril, 1854) (n=1), P. olf-ersii (Lichtenstein, 1823) (n=4), P. patagoniensis (Girard, 1858) (n=6), Erythrolamprus poecilogyrus (Wied-Neuwied, 1825) (n=10), E. jaegeri (Günther, 1858) (n=2), Atractus reticulatus (Boulenger, 1885) (n=1), Dipsas ventrimaculatus (Boulenger, 1885) (n=3), Thamnodynastes strigatus (Günther, 1858) (n=2), Phalotris lemniscatus (Duméril, Bibron & Duméril, 1854) (n=1) (Dipsadidae) and Bothrops alternatus (Duméril, Bibron & Duméril, 1854) (n=6) (Viperidae). The snakes came from the municipalities of Capão do Leão (31° 45’ 48” S - 52° 29’ 02” W), Pelotas (31° 46’ 19 “S - 52° 20’ 33 “W), Rio Grande (32° 02’ 06 “S - 52° 05’ 55 “W), Encruzilhada do Sul (30° 32’ 38 “S - 52° 31’ 19 “W) and Dom Pedrito (30° 58’ 58 “S - 54° 40’ 23 “W), Rio Grande do Sul. Fifty of them were collected dead on roads from March 2017 to June 2019. The collection of specimens were licensed by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio No. 38913). Four snakes were donated by the Núcleo de Reabilitação da Fauna Silvestre e Centro de Triagem de Animais Silvestres of the Federal University of Pelotas (NURFS-CE-TAS/UFPel), where they died after a rehabilitation attempt. The other hosts were donated by the Ver-tebrate Laboratory of the Federal University of Rio Grande (n= 36) and Vertebrate Zoology Laboratory of the Federal University of Pelotas (n= 11), where the specimens were fixed in formalin and conserved in 70°GL alcohol.The hosts were necropsied for analysis of the coelomic cavity. The larvae were fixed in AFA, con-served in 70°GL alcohol and clarified with Amann lactophenol for morphological identification accord-ing to Measures (1988).  The parasitological indices were calculated according to Bush et al. (1997).  The specimens were deposited in the helminth collec-tion of the Laboratory of Wild Animal Parasitology (CHLAPASIL n° 831-836). The photomicrographs were done in an Olympus® BX 41 microscope with attached camera system and the images were pre-pared in Adobe Photoshop® CS5. Among the total hosts examined, six (5.9%) were parasitized by fourth stage larvae of Eustron-gylides sp. (Fig. 1), which were found in the coelo-mic cavity of Helicops infrataeniatus (Fig. 2), with a prevalence of 9.2% and mean intensity of infection of 1.83 helminths/host. Female larvae were larger than male larvae, which measured 75-115 mm and 65-80 mm length, respectively.Helicops infrataeniatus is a non-venomous aquatic snake that can reach about one meter in length. It is distributed in southern Brazil, Paraguay, Uruguay and Argentina (Quintela and Loebmann, 2009; Abegg and Entiauspe-Neto, 2012). The diet of the species includes mostly fish and amphibians (Aguiar and Di-Bernardo, 2004), which were pos-sibly the source of infestation of the snakes in this study. The transmission of Eustrongylides species occurs through the trophic chain involving aquatic organisms such as oligochaetes (primary interme-diate hosts), fish, anurans, snakes (secondary and/or paratenic intermediate hosts) and birds (definitive hosts). Bird infection occurs by ingestion of the in-fective fourth-stage larva present in the secondary and/or paratenic intermediate hosts (Measure, 1988; Moravec, 1994; Friend and Franson, 1999). Larvae are often found parasitizing several fish species in Brazil, such as Hoplias malabaricus (Bloch, 1794) (Characiformes), Cichla piquiti Kullander & Ferreira, 2006 and Plagioscion squamosissimus (Heckel, 1840) (Perciformes) (Isaac et al., 2004; Mar-tins et al., 2009; Meneguetti et al., 2013; Carvalho et al., 2017). Amphibians were also reported as hosts of Eustrongylides larvae in northern Brazil (Melo et 153Cuad. herpetol. 35 (1): 151-155 (2021)al., 2016). There are no previous records of larvae of this nematode associated with snakes in Brazil; how-ever, there are records in North America (Bursey, 1986), Europe (Mihalca et al., 2007; Biserkov, 1995; Yildirimhan et al., 2007) and Australia (Lichtenfels and Lavies, 1976; Jones, 1978).Snakes can include in their diet of large variety of vertebrates (Voris and Murphy, 2002; Abegg et al., 2005; Costa et al., 2009), enabling the transmis-sion of parasites through complex trophic networks (Marcogliese, 2004). Herons, such as Syrigma sibila-trix (Temminck, 1824) (Ardeidae) feed on Helicops infrataeniatus as observed by Franz et al. (2007) in Campo Belo do Sul in the state of Santa Catarina, Brazil. In the region of our present study, Eustron-gylides ignotus was reported in herons Ardea cocoi Linnaeus, 1766 and Nycticorax nycticorax (Linnaeus, 1758) (Ardeidae) (Bernardon et al., 2017), and lar-vae of this nematode were found in siluriform fish, Callichthys callichthys (Linnaeus, 1758), as well as in Hoplias malabaricus (Carolina Silveira Mascarenhas, com. pess.). The record of fourth stage larvae of Eustrongylides sp. in H. infrataeniatus suggests that the species may act as a trophic bridge in the para-site cycle, since the snake has aquatic habits, feeds on fish and serves as a food resource for birds such as herons. These records highlight the importance of the region for maintenance of the Eustrongylides species life cycle and warns about the presence of a nematode with zoonotic potential (Eiras et al. 2016).Figure 1. Fourth stage larvae from Eustrongylides sp. (Enoplida: Dioctophymatidae) found in the coelomic cavity of Helicops infra-taeniatus Jan, 1865 (Serpentes: Dipsadidae) in the extreme south of Brazil. A - Anterior extremity of female larva (Arrows indicate the cephalic papillae; oe: esophagus; bar – 100 μm). B - Posterior extremity of the female larva (Arrows indicate the primordial vulvar; bar - 100μm). C - Arrows indicate cuticle layers (oe: esophagus; bar - 12,5 μm). D - Posterior end of the male larva (bar – 60 μm).154J. V. Pereira et al. - Eustrongylides sp. larvae in snakesIt is important to point out that the other snakes used in this study present predominantly terrestrial habits, such as Bothrops alternatus, Thamnodynastes strigatus, Philodryas patagoniensis, or semi-aquatic habit as Erythrolamprus jaegeri and E. poecilogyrus (Achaval and Olmos, 2003), which may hinder or even make completely impossible the transmission of this nematode. However, future studies should be conducted to complement the results presented herein to help in the understanding of parasitic relationships involving Eustrongylides species and snakes in the Neotropical region.The occurrence of Eustrongylides larvae in Helicops infrataeniatus registered for the first time, is the second finding of helminths parasitizing this species in Brazil, since there is a previous record of parasitism by Opisthogonimus serpentis Artigas, Ruiz & Leão 1943 (Digenea: Opsitogonimidae) (Fernandes and Kohn, 2014).AcknowledgmentsSpecial thanks to José Dornelles, Daniel Loebmann, Rafael Dias, Marco Coimbra, Juliana Wolter and Ricardo da Silva for their assistance. This work was supported by CAPES (Coordenação de Aper-feiçoamento do Pessoal de Nível Superior, process number 32/2010) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) through scholarship to JVP.Literature citedAbegg, A.D.; Entiauspe-Neto, O.M. 2012. Serpentes do Rio Grande do Sul. Tapera: Livraria & Editora Werlang.Abegg, A.D.; Entiauspe-Neto, O.M.; Costa, H.C. & Santos, P.S. 2015. Erythrolamprus poecilogyrus sspp. (Serpentes: Dipsadidae): predação. Herpetologia Brasileira 4: 60-63.Achaval, F. & Olmos, A. 2003. Anfíbios y Reptiles del Uruguay. Graphis, Montevideo.Aguiar, L.F.S. & Di-Bernardo, M. 2004. Diet and feeding behavior of Helicops infrataeniatus (Serpentes: Colubridae: Figure 2. Eustrongylides sp. fourth stage larva (Enoplida: Dioctophymatidae) found in the coelomic cavity of Helicops infrataeniatus Jan, 1865 (Serpentes: Dipsadidae) in the extreme south of Brazil (Bar – 12 mm).155Cuad. herpetol. 35 (1): 151-155 (2021)Xenodontinae) in Southern Brazil. Studies on Neotropical Fauna and Environment 39: 7-14.Bernardon, F.F.; Valente, A.L.S. & Müller, G. 2017. Helminth assemblage of aquatic birds (Pelecaniformes: Ardeidae) of southern Rio Grande and a checklist of helminths of herons of Brazil. Neotropical Helminthology 11: 357-375.Biserkov, V.Y. 1995. 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First record of Eustrongylides sp. (Nematoda: Dioctophymatidae) larvae parasitizing snakes in the Neotropical region

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First record of Eustrongylides sp. (Nematoda: Dioctophymatidae) larvae parasitizing snakes in the Neotropical region

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