117 Gastrointestinal Parasitism in Rescued Wild Birds Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Neotropical Helminthology Neotropical Helminthology, 2024, vol. 18 (2), 117-126 ORIGINAL ARTICLE / ARTÍCULO ORIGINAL FAR FROM HOME? A NEW LOCALITY RECORD OF FALCAUSTRA SANJUANENSIS GONZÁLEZ, SANABRIA & QUIROGA, 2013 (NEMATODA: KATHLANIIDAE) IN A NEW HOST FROM THE BRAZILIAN AMAZON¿LEJOS DE CASA? UN NUEVO REGISTRO DE LOCALIDAD DE FALCAUSTRA SANJUANENSIS GONZÁLEZ, SANABRIA & QUIROGA, 2013 (NEMATODA: KATHLANIIDAE) EN UN NUEVO HUÉSPED DE LA AMAZONÍA BRASILEÑA Leandro Mauricio Oliveira Silva 1* ,Ronald Ferreira Jesus 1 , Bianca Nandyara 1 , Yuri Willkens 1 , Lorena Freitas Souza Tavares-Costa 1 , Jeannie Nascimento Santos 1 & Francisco Tiago Vasconcelos Melo 1 ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403 DOI: https://dx.doi.org/10.62429/rnh20242181781 Universidad Nacional Federico Villarreal Volume 18, Number 2 (jul - dic) 2024 Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto, distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original. ABSTRACT Studies on the helminth parasites of South American freshwater turtles are rare and punctual. T e parasitic fauna of Kinosternon scorpioides Linnaeus, 1766 nematodes from Brazil is restricted to only 4 species: Serpinema magathi Sprehn, 1932, Serpinema monospiculatus Freitas & Dobbin Jr., 1971 , Serpinema pelliculatus Silva, Jesus & Melo, 2023 and Spiroxys f gueiredoi Freitas & Dobbin Jr., 1962 . T e present work aimed to report the occurrence of the species Falcaustra sanjuanensis González, Sanabria & Quiroga, 2013 (Nematoda: Kathlaniidae), a parasite of an anuran from Argentina, in the large intestine of K. scorpioides from the Brazilian Amazon. T e specimens of freshwater turtles were collected, anesthetized, and euthanized; the nematodes found were f xed in 90°GL ethanol and analyzed by light microscopy and scanning electron microscopy. T e nematodes showed some morphological and morphometric variations when compared with the original description of the species. Here we present new locality and host records for F. sanjuanensis and a new parasite record for K. scorpioides from Brazil. 1 Laboratório de Biologia Celular e Helmintologia “Profa. Dra. Reinalda Marisa Lanfredi”, Instituto de Ciências Biológicas, Universidade Federal do Pará (UFPA), Av. Augusto Correa 01, Guamá Zipcode: 66075110 – Belém, Pará, Brasil. * Corresponding author: leandro97oliveirasilva@gmail.com Leandro Mauricio Oliveira Silva: https://orcid.org/0000-0003-1123-143XRonald Ferreira Jesus: htt-ps://orcid.org/0000-0001-5067-0879Bianca Nandyara: https://orcid.org/0000-0002-1342-1328Yuri Willkens: https://orcid.org/0000-0002-0904-5200Lorena Freitas Souza Tavares-Costa: https://orcid.org/0000-0002-7518-628XJeannie Nascimento Santos: https://orcid.org/0000-0002-6612-6410Francisco Tiago Vasconcelos Melo: https://orcid.org/0000-0001-8935-2923
118 Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Silva et al. Keywords : Brazilian Amazon – Falcaustra sanjuanensis – Kathlaniidae – Kinosternon scorpioides – morphology – Turtle parasites RESUMEN Los estudios sobre los helmintos parásitos de las tortugas de agua dulce de América del Sur son escasos y puntuales. La fauna parasitaria de los nematodos de Kinosternon scorpioides Linnaeus, 1766 de Brasil está restringida a solo cuatro especies: Serpinema magathi Sprehn, 1932, Serpinema monospiculatus Freitas & Dobbin Jr., 1971, Serpinema pelliculatus Silva, Jesus & Melo, 2023 y Spiroxys Figueiredoi Freitas & Dobbin Jr., 1962 . El objetivo del presente trabajo fue reportar la ocurrencia de la especie Falcaustra sanjuanensis González, Sanabria & Quiroga, 2013 (Nematoda: Kathlaniidae), parásito de un anuro de Argentina, en el intestino grueso de K. scorpioides de la Amazonía brasileña. Los ejemplares de tortugas de agua dulce fueron colectados, anestesiados y sacrifcados; los nematodos encontrados se fjaron en etanol 90°GL y se analizaron mediante microscopía óptica y microscopía electrónica de barrido. Los nematodos mostraron algunas variaciones morfológicas y morfométricas al compararlos con la descripción original de la especie. Aquí presentamos nuevos registros de localidad y hospedante para F. sanjuanensis y un nuevo registro de parásito para K. scorpioides de Brasil. Palabras clave : Amazonía Brasileña - Falcaustra sanjuanensis - Kathlaniidae - Kinosternon scorpioides – morfología - Parásitos de tortugas INTRODUCTION Vertebrate helminth parasites are a widely diverse but still poorly understood group. Tese organisms represent an important component of ecosystems and play vital ecological roles, impacting the structure and dynamics of food webs and contributing to biodiversity and the functioning of ecological communities (Poulin & Morand, 2000; Hugot et al ., 2001; Buck, 2019; Juaréz-Estrada et al ., 2023; Lymbery & Smit, 2023).Recently, many studies describing species of amphibian and reptile parasites have been developed; however, there is still a considerable gap in knowledge about the parasite diversity of turtles (Anjos, 2011). Studies on the helminth biodiversity of South American turtles are relatively recent and are generally represented by specifc research in some countries such as Brazil, Uruguay, and Peru (Mascarenhas & Müller, 2021). Kinosternon scorpioides Linnaeus, 1766 is a freshwater turtle belonging to the Family Kinosternidae Agassiz, 1857, widely distributed throughout the American continent, occurring from southern Mexico to northern Argentina (Turtle Taxonomic Work Group, 2017). Te species is oviparous, has semi-aquatic and nocturnal habits, and prefers to inhabit clear water environments, but it can also occur in black waters (Ferrara et al ., 2017).In general, studies with K. scorpioides are directed to anatomical, food, ecological, and reproductive analyses, aiming at the monitoring, conservation, and management of this species, but parasitological data are still very scarce (Araújo et al ., 2013; Sousa et al., 2014; Chaves et al ., 2020; Ferreira et al ., 2020; Santos et al., 2021).Between the various groups of parasitic helminths, nematodes are the most found in turtles. Amidst them, the family Kathlaniidae Lane, 1914 is one of the most diversifed, with the genus Falcaustra Lane, 1915 has about 100 parasitic species from the digestive tract of amphibians, fshes, and reptiles (Baker, 1986).Currently, 12 valid species of the genus Falcaustra occur in the Neotropical region, namely: F. belemensis Baker & Bain, 1981; F. caballeroi (Caballero, 1935) Chabaud & Golvan, 1957; F. condorcanquii Ibanez & Córdova 1976; F. costaricae Bursey, Goldberg & Miller, 2004; F. guanacastensis Bursey & Brooks, 2011; F. guatamalana (Caballero, 1953) Chabaud & Golvan, 1957; F. intermedia (Caballero, 1939) Freitas & Lent, 1941; F. mascula (Rudolphi, 1819) Freitas & Lent, 1941; F. pumacahuai Ibanez & Córdova 1976; F. sanjuanensis González, Sanabria & Quiroga, 2013; F. tiahuanaquensis Ibanez & Córdova 1976; and F. tikasinghi (Schoenecker, Schmidt & Everard, 1977) Baker & Bain, 1981 (Freitas & Lent, 1941; Chabaud & Golvan, 1957; Baker & Bain, 1981; Bursey et al ., 2004; Bursey & Brooks, 2011; González
119 Far from home? A new locality record of Falcaustra sanjuanensis Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 et al ., 2013). Of those, F. guanacastensis , F. intermedia, and F. tikasinghi are the only found in turtles, with no record of this genus parasitizing Kinosternon from Brazil (Mascarenhas & Müller, 2021). Falcaustra sanjuanensis was described as parasitizing the large intestine of the anuran Odontophrynus cf. barrioi Cei, Ruiz & Beçak, 1982 from Argentina, which is the only record. In the present study, we found specimens of this nematode species in the large intestines of K. scorpioides from Brazil. Tus, we provide new morphological and morphometric data for F. sanjuanensis , a new location and host record. MATERIAL AND METHODS During an expedition to collect helminth parasites from amphibians and reptiles in Serra dos Carajás, Pará, Brazil (6°6’29”S 50°18’16”W), 4 specimens of K. scorpioides were collected (under SISBIO collection license: 53527-7), sent to the laboratory, anesthetized and euthanized. Te nematodes collected from the large intestine were washed in 0.9% saline solution and fxed in 90°GL ethanol. For morphological and morphometric analysis, the nematodes were clarifed in 50% Amann’s lactophenol, mounted on temporary slides, and examined in an Olympus BX41 optical microscope (Olympus, Tokyo, Japan) with a drawing tube attached.For scanning electron microscopy (SEM), 6 specimens of nematodes (3 males and 3 females) were postfxed in 1% OsO4, dehydrated in an ascending series of ethanol, critically dried with CO 2 , coated with gold-palladium, mounted on metallic supports, and analyzed in a Vega3 microscope (TESCAN, Brno, Czech Republic) with acceleration voltage between 10-20 kV.Measurements are presented in micrometers unless otherwise indicated, with the mean value followed by the minimum and maximum values in parentheses. Te voucher specimens were deposited in the Collection Other Invertebrates of the Museu Paraense Emílio Goeldi (MPEG), Pará, Brazil. Ethical aspects : All procedures contributing to this work comply with all applicable institutional, national, and international guidelines for animal care and use Animal Research Ethics Committee, Federal University of Pará, under license N8341260821CEUA/UFPa. Te present study was approved by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Brazil, and host specimens were collected under license number SISBIO: 53527-7. RESULTS Family Kathlaniidae Lane, 1914Genus Falcaustra Lane, 1915 Falcaustra sanjuanensis González, Sanabria & Quiroga, 2013 (Figs. 1, 2) General description: Large-sized nematodes; cylindrical body, robust. Cuticle with fne transverse striations. Truncated anterior end (Fig. 1A). Lateral alae absent. Triangular mouth opening, surrounded by 3 large lips; 2 papillae on each lip, 1 amphid on each subventral lip (Figs. 1B, 2A). Short, muscular pharynx. Divided esophagus, with elongated body, subspherical isthmus, spherical bulb, opening to the intestine through a valve (Fig. 1A). Nerve ring located in the frst third of the esophageal body. Deirids positioned in the posterior half of the esophageal body (Fig. 1A). Small excretory pore posterior to deirids (Figs. 1A, 2B). Short tail (Figs. 1E, 1G, 2D, 2E). Males (based on 10 adult specimens): Body length 11.21 (9.93–12.41) mm. Width at esophagus-bowel junction 355 (300–394). Pharynx 78 (63–100) × 83 (63–100). Esophagus (except isthmus and bulb) 1.54 (1.32–1.66) mm × 101 (89–111). Isthmus 128 (103–152) × 114 (95–126). Bulb 210 (176–232) × 193 (168–216). Nerve ring, deirids and excretory pore located at 380 (345–426), 1.12 (0.97–1.26) mm and 1.27 (1.09–1.40) mm, respectively, from the anterior end. Well-developed pre-cloacal musculature; pre-cloacal pseudosucker present (Fig. 1E), length 387 (307–453). Distance from the beginning of the pseudosucker to the tail 2.86 (2.54–3.07) mm. Tail length 459 (395–495) (Fig. 1E). Eleven pairs of caudal papillae: 3 pre-cloacal, 2 ad-cloacal (1 anterior and 1 posterior to the cloaca), 6 post-cloacal (frst ventral pair, second lateral pair located near the cloaca; third subventral pair near the middle of the tail; fourth dorsoventral pair, ffth lateral pair, sixth dorsoventral pair located near the posterior end); single median papilla immediately anterior to the cloacal opening (Figs. 1D, 2D, E). Gubernaculum length 208 (175–245) (Fig. 1F). Equal spicules, length 1.25 (1.18–1.32) mm (Fig. 1H). Females (based on 11 adult specimens): Body length 12.58 (10.68–14.23) mm. Width at esophagus-intestine junction 366 (315–421). Pharynx 83 (63–116) × 87 (79–111). Esophagus (except isthmus and bulb) 1.72 (1.60–1.88) mm × 115 (95–153). Isthmus 148 (135–158) × 132 (116–153). Bulb 208 (179–242) × 204 (184–232). Nerve ring, deirids and excretory pore located 411 (384–453), 1.19 (1.09–1.33) mm and 1.37 (1.25–1.55) mm, respectively, from the anterior end. Vulva at the posterior
120 Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Silva et al. half of the body, 4.70 (4.20–5.13) mm from the posterior end (Fig. 2C). Tail length 640 (595–695) (Figs. 1G, 2F). Vulva-anus distance 4.09 (3.57–4.59) mm. Oviparous. Uterus with several eggs (Fig. 1C). Tick-shelled, non-embryonic eggs, length 79 (74–85), width 57 (46–61) (Fig. 1I). Figure 1. Light microscopy of Falcaustra sanjuanensis González, Sanabria & Quiroga, 2013 parasite of K. scorpioides . A, Anterior extremity of male, ventral view; B, Cephalic extremity, apical view; C, Uterine region, side view; D, Posterior extremity of male, distribution of caudal papillae, ventral view; E, Posterior end of male, side view; F Gubernaculum, side view; G, Spicules, side view; H, Posterior extremity of female, side view; I, Eggs, front view. Scale-bars : A, C, D, E, G, H, 350 µm; B, F, 50 µm; I, 25 µm.
121 Far from home? A new locality record of Falcaustra sanjuanensis Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Figure 2. Scanning Electron Microscopy of Falcaustra sanjuanensis González, Sanabria & Quiroga, 2013 parasite of K. scorpioides . A, Cephalic end, apical view, showing cephalic papillae (arrow) and amphid (asterisk); B, Anterior extremity, ventrolateral view, excretory pore and deirid; C, Female, ventral view, vulva; D, Female, ventral view, anus and tail; E, Posterior region of the male, distribution of the caudal papillae (arrow). Inset: detail of the deirid and papillae near the tip of the tail (arrow). Abbreviations: De, deirid; Ep, excretory pore; Vu, vulva; An, anus. Scale-bars : A, 20 µm; B, 100 µm; Inset, 5 µm; C, D, E, 100 µm; Inset, 50 µm.
122 Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Silva et al. Taxonomic summary Host: Kinosternon scorpioides Linnaeus, 1766Location: Serra dos Carajás (6°6’29”S 50°18’16”W), Pará, Brazil.Voucher specimens: 10 males (MPEG 291) and 11 females (MPEG 292) deposited in the Collection Other Invertebrates of the Museu Paraense Emílio Goeldi.Site of infection: Large intestine.Prevalence: 4 infected hosts out of 4 analyzed (100%). DISCUSSION Falcaustra sanjuanensis was described as parasitizing the large intestine of Odontophrynus cf. barrioi , an anuran typical of arid and semiarid environments, in Pie de Palo, Quebrada de las Flores, Province of San Juan, Argentina. We found 34 specimens (16 males and 18 females) of this nematode in the large intestines of K. scorpioides from Brazil. Te morphological and morphometric characteristics of these nematodes are similar to those reported in the original description. However, in our study, we also describe the deirids, which was not observed by Gonzalez et al . (2013).According to Anderson et al . (2009), the presence of an oral opening with 3 well-developed lips, an esophagus with a short anterior pharynx, and a subspherical isthmus slightly anterior to the esophageal bulb are the main diagnostic characteristics of Falcaustra . Te species of the genus are diferentiated mainly by the distribution of caudal papillae, length of the spicules, and the presence or absence of a pseudosucker (Bursey & Brooks, 2011). Among the 12 known species of the genus only F. condorcanquii , F. intermedia , F. mascula , F. pumacahuai , F. sanjuanensis and F. tiahuanaquensis have a pseudosucker. Falcaustra sanjuanensis have similar length of spicules when compared to F. mascula , but it is longer than in F. pumacahuai and F. tiahuanaquensis , and smaller than F. condorcanquii and F. intermedia . Additionally, F. sanjuanensis difers from all those mentioned species with pseudosucker by having a diferent male caudal papillae number and arrangement. Among non-Neotropical Falcaustra species, F. sanjuanensis only resembles F. andrias (He, Liu & Ma, 1992) Liu, Zhang & Zhang, 2011 and F. longispicula Walton, 1927 by the pattern of caudal papillae. Falcaustra andrias from the Oriental realm has pseudosucker but difer by some metric data: smaller body length of males (9.93–12.41 mm in F. sanjuanensis vs. 5.47–7.78 mm) and females (10.68–14.23 mm in F. sanjuanensis vs. 7.60 –8.08 mm); smaller spicules length (1.18-1.32 mm in F. sanjuanensis vs. 0.48 to 0.57 mm); and length of the gubernaculum (175-245 in F. sanjuanensis vs. 100-109). Furthermore, these species have a diferent arrangement of post-cloacal papillae (frst ventral pair, second lateral pair; third subventral pair; fourth dorsoventral pair, ffth lateral pair and sixth dorsoventral pair vs. 3 ventral pairs and 3 lateral pairs). Falcaustra longispicula from the Nearctic realm resembles F. sanjuanensis from the present study by the length of spicules (1.18–1.32 mm vs. 1.20–1.21 mm). However, it has a larger length of spicules when compared to F. sanjuanensis described by González et al. (2013). Additionally, F. longispicula difer by the absence of pseudosucker, which is present in F. sanjuanensis. SEM helped us to add new ultrastructural observations to F. sanjuanensis described by González et al. (2013). We observed details of the oral opening and the presence of deirids, positioned in the posterior half of the anterior end. Te distribution of the caudal papillae was also an important morphological characteristic observed by SEM to reinforce the similarity between the specimens found in Argentina and specimens from Brazil. Finally, we also obtained ultrastructural details of the excretory pore, vulva, anus, and tail. Specimens of F. sanjuanensis from K. scorpioides show some intraspecifc variations in metric data when compared to measurements presented by Gonzalez et al. (2013). In our specimens, males have shorter isthmus length (103–152 vs. 150–200), and longer spicules (1.18–1.32 mm vs. 0.45–0.67 mm) and tail (395–495 vs. 260–370); while in females the width of the pharynx (79–111 vs. 53–73) and the lengths of the tail (595–695 vs. 280–500) and eggs (74–85 vs. 63–72) are larger than in F. sanjuanensis described by González et al . (2013). Furthermore, the specimens described in our study have the largest spicule among the Falcaustra species with pseudosucker, and the second largest spicule among the neotropical species (Table 1). González-Solís & Moravec (2004) suggest that intraspecifc morphological and biometric variability among parasitic nematodes may be associated with the host’s local ecological conditions. However, both the type locality and the new locality presented in this study are regions of mountain ranges, with similar climates, indicating that perhaps other factors are also related to these morphological and metric variations between specimens.
123 Far from home? A new locality record of Falcaustra sanjuanensis Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Table 1. Morphometric data of Falcaustra sanjuanensis from the original description and the present study. Falcaustra sanjuanensis (present study) Falcaustra sanjuanensis (González et al ., 2013)Host Kinosternon scorpioidesOdontophrynus cf. barrioi LocalityBrazilArgentinaSexMaleFemaleMaleFemaleBody length (mm)9.93–12.4110.68–14.2311.17–13.4510.10–15.50Body width at esophagus-bowel junction300–394315–421270–415310–485Pharynx length×width63–100×63–10063–116×79–11186–110×50–7285–110×53–73Esophagus (except isthmus and bulb) length(mm)×width1.32–1.66×89–1111.60–1.88×95–1531.55–1.94×50–981.67–1.98×60–100Isthmus length×width103–152×95–126135–158×116–153150–200×90–150125–200×100–150Bulb length×width176–232×168–216179–242×184–232160–215×170–215160–250×160–230Nerve ring*345–426384–453350–460370–450Deirids (mm)*0.97–1.261.09–1.33––Excretory pore (mm)*1.09–1.401.25–1.551.06–1.551.18–1.64Tail length395–495595–695260–370280–500Pseudosucker length307–453–250–450–Gubernaculum length175–245–175–230–Spicules length1.18–1.32–450–675–Vulva (mm)*–4.20–5.13–3.0-5.4Vulva-anus distance–3.57–4.59––Eggs length–74–85**–63–72Eggs width–46–61**–50–58 *Distance from the anterior end.** Measurmentss based on the average of 10 eggs from each specimen analyzed.
124 Neotropical Helminthology (Lima). Vol. 18, Nº2, jul - dec 2024 Silva et al. We consider plausible the hypothesis that F. sanjuanensis has switched from a chelonian (ancestral host) to an anuran (new host) since turtles originated frst. For the host-switching, both hosts must coexist in an ecosystem, enabling the parasite to shift (Araujo et al., 2015). Kinosternon scorpioides is widely distributed in South America, even in Argentina, the type locality of F. sanjuanensis , described parasitizing an anuran of the genus Odontophrynus Reinhardt & Lütken, 1862. Both hosts have aquatic habits and have relatively similar ecological niches and eating habits, which may increase the possibility of sharing the parasites among these animals (Aho, 1990).When a parasite changes its host and colonizes a diferent niche, it enriches the local biodiversity and if this change is accompanied by strong isolation from the ancestral host, it favors genetic diferentiation and possible speciations (Jaramillo & Rivera-Parra, 2018). However, it is possible that the host switch event of the nematode F. sanjuanensis was relatively recent and, therefore, possible genetic alterations have not yet manifested themselves phenotypically to the point where we consider that there was a morphological diferentiation among diferent populations of this parasite species.Another hypothesis is that the phenomenon of “ecological conservatism” has occurred, in which the exchange of hosts overcomes cospeciation; that is, the parasite manages to establish a host exchange but does not undergo changes. Falcaustra sanjuanensis managed to expand its distribution once it acquired a new host but remained morphologically indistinct from the parasites of the ancestral host. Tus, the interaction with a new vertebrate host taxon does not seem to have hampered the parasite’s distribution, indicating that it is probably an organism with more generalist characteristics (Hoberg & Brooks, 2008).To date, 8 species of nematodes have been reported in K. scorpioides , named: Atractis impura Caballero, 1944; Klossinemella caballeroi Brenes & Bravo-Hollis, 1960; Serpinema kachugae Baylis & Daubney, 1922; Serpinema magathi Sprehn, 1932; Serpinema monospiculatus Freitas & Dobbin Jr., 1962; Serpinema pelliculatus Silva, Jesus & Melo, 2023; Spiroxys fgueiredoi Freitas & Dobbin Jr.,1962; and Capillaria sp. (Alho, 1965; Brenes & Bravo-Hollis, 1960; Freitas & Dobbin Jr., 1971; Hungría, 1978; Bursey & Brooks, 2011; Viana et al., 2016; Pereira et al ., 2018; Silva et al ., 2023). Terefore, in this study, we present new morphologic data, location records, and a new host for the F. sanjuanensis species. Author contributions: CRediT (Contributor Roles Taxonomy)LMOS = Leandro Mauricio Oliveira Silva RFJ = Ronald Ferreira Jesus BN = Bianca Nandyara YW = Yuri Willkens LFSTC = Lorena Freitas Souza Tavares-Costa JNS = Jeannie Nascimento Santos FTVM = Francisco Tiago Vasconcelos Melo Conceptualization: LMOS, RFJ, FTVM Data curation: LMOS, RFJ, FTVM Formal Analysis: LMOS, RFJ, FTVM Funding acquisition: JNS, FTVM Investigation: LMOS, RFJ, FTVM Methodology: LMOS, RFJ, BN, YW, LFSTC, FTVM Project administration: LMOS, RFJ, FTVM Resources: JNS, FTVM Software: YW, LFSTC Supervision: LMOS, RFJ, BN, LFSTC, JNS, FTVM Validation: LMOS, RFJ, FTVM Visualization: LMOS, RFJ, BN, FTVM Writing – original draft: LMOS, RFJ, BN, FTVM Writing – review & editing: LMOS, RFJ, FTV ACKNOWLEDGEMENTS We are grateful to Ana Nunes dos Santos and Fred Gabriel Haick de Moura for his support in the hosts’ necropsies and in the collection of nematodes. We are grateful to Edilene Oliveira da Silva, from the Laboratory of Cellular Structural Biology at the Federal University of Pará, Belém, for her technical support in the SEM analysis. Tis study was funded by the Coordination for the Improvement of Higher Education Personnel (CAPES) / PPGBAIP / UFPA and the National Council for Scientifc and Technological Development (CNPq) (process number 431809 / 2018-6 Universal); CNPq research productivity scholarship for MELO, F.T.V. (Case number 304955 / 2018-3) and SANTOS, J.N. (Case number 305552 / 2019-8). Tis study is part of the Ph. D. thesis of Leandro Mauricio Oliveira da Silva from the Postgraduate Program in Biology of Infectious and Parasitic Agents (PPGBAIP) at ICB-UFPA.
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