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A new species of Kalicephalus (Nematoda: Diaphanocephalidae), a parasite of Bothrops atrox (Serpentes: Viperidae) from the Brazilian Amazon

Published online by Cambridge University Press:  11 July 2025

F.G. Haick Open the ORCID record for F.G. Haick [Opens in a new window] ,
L.F.S. Tavares-Costa Open the ORCID record for L.F.S. Tavares-Costa [Opens in a new window] ,
G.L. Rebêlo Open the ORCID record for G.L. Rebêlo [Opens in a new window] ,
J.K.S. Neves Open the ORCID record for J.K.S. Neves [Opens in a new window] ,
A.J.S. Félix Open the ORCID record for A.J.S. Félix [Opens in a new window] ,
M.I. Müller Open the ORCID record for M.I. Müller [Opens in a new window] ,
L.F.F. Trindade Open the ORCID record for L.F.F. Trindade [Opens in a new window] ,
C.E. Costa-Campos Open the ORCID record for C.E. Costa-Campos [Opens in a new window] ,
G.F. Maschio Open the ORCID record for G.F. Maschio [Opens in a new window]  and
F.T.V. Melo Open the ORCID record for F.T.V. Melo [Opens in a new window]
F.G. Haick
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
L.F.S. Tavares-Costa
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
G.L. Rebêlo
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
J.K.S. Neves
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
A.J.S. Félix
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
M.I. Müller
Affiliation:
Oregon State University, Department of Microbiology, Corvallis, OR, 97331, USA
L.F.F. Trindade
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
C.E. Costa-Campos
Affiliation:
Laboratory of Herpetology, Department of Biological and Health Sciences, Federal University of Amapá (UNIFAP), Jardim Marco Zero, Rod. Juscelino Kubitschek, km 02, Macapá, Amapá 68903‑419, Brazil
G.F. Maschio
Affiliation:
Laboratory of Ecology and Zoology of Vertebrates, Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
F.T.V. Melo*
Affiliation:
Laboratory of Cellular Biology and Helminthology “Profa. Dra. Reinalda Marisa Lanfredi” –Institute of Biological Sciences, https://ror.org/03q9sr818 Federal University of Pará (UFPA) , Av. Augusto Correa 01, Guamá, Belém, Pará 66075‑110, Brazil
*
Corresponding author: F.T.V. Melo; Email: ftiago@ufpa.br
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Abstract

Kalicephalus (Molin, 1861) comprises 33 species of gastrointestinal snake and lizard parasites with a cosmopolitan distribution, with seven taxa occurring in the Neotropical realm. In the present study, we describe Kalicephalus atroxi n. sp., found parasitising the snake Bothrops atrox, from the Eastern Amazon in the State of Amapá, North of Brazil. We used an integrative approach that included light microscopy, scanning electron microscopy, and sequencing of the internal transcribed spacer 1 (ITS1) region to describe Kalicephalus atroxi n. sp. The new species has a buccal capsule characteristic of the genus, a slight cuticular inflation in the cephalic region. The females have an amphidelphic reproductive system, a vulva with prominent lips, and a long tail, tapering posteriorly. The males have long and alate spicules, and the copulatory bursa is lobed with dorsal rays with distinct morphology compared to their congeners. Molecular analyses and phylogenetic reconstructions cluster the new species into a well-supported clade with K. costatus costatus, from Chironius fuscus, from the same locality in northern Brazil. Kalicephalus atroxi n. sp. is the eighth species of the genus in the Neotropics, the seventh in Brazil, the second described parasitising B. atrox in Brazil, and the first species of snake nematode described in the State of Amapá.

Keywords

AmazonViperidaeNematodataxonomymolecular

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Type
Research Paper
Information
Journal of Helminthology , Volume 99 , 2025 , e76
Copyright
© The Author(s), 2025. Published by Cambridge University Press

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References

Anderson, RC (2000) Nematode Parasites of Vertebrates. Their Development and Transmission. 2nd edition. Wallingford, Oxon: CABI Publishing, 43–44.10.1079/9780851994215.0000CrossRefGoogle Scholar
Chilton, NB, Huby-Chilton, F, Gasser, RB and Beveridge, I (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetics and Evolution 40(1), 118–128. https://doi.org/10.1016/j.ympev.2006.01.003CrossRefGoogle ScholarPubMed
Cunha, OR and Nascimento, FP (1975) Ofídios da Amazônia VII—as serpentes peçonhentas do gênero Bothrops (jararacas) e Lachesis (surucucu) da região leste do Pará. (Ophidia, Viperidae). Boletim do Museu Paraense Emílio Goeldi 83, 1–42. https://repositorio.museu-goeldi.br/handle/mgoeldi/763Google Scholar
Edgar, RC (2004) Muscle: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5(113), 1–19. https://doi.org/10.1186/1471-2105-5-113CrossRefGoogle ScholarPubMed
Fraga, R, Lima, AP, Prudente, AL and Magnusson, WE (2013) Guia de cobras da região de Manaus – Amazônia Central. Editora INPA, Manaus.Google Scholar
González, CE, Schaefer, EF and Duré, MI (2018) Presence of Kalicephalus subulatus Molin, 1861 (Nematoda, Diaphanocephalidae) in Wagler’s snake, Xenodon merremi from Argentina. Annals of Parasitology 64(4), 399–405. https://doi.org/10.17420/ap6404.177Google ScholarPubMed
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52(1), 696–704. https://doi.org/10.1080/10635150390235520CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199CrossRefGoogle ScholarPubMed
Kuzmin, Y, Kinsella, JM, Tkach, VV and Bush, SE (2013) New species of Kalicephalus (Nematoda: Diaphanocephalidae) from a snake, Oxyrhabdium leporinum, on Luzon Island, Philippines. Comparative Parasitology 80(2), 240–246. https://doi.org/10.1654/4636.1CrossRefGoogle Scholar
Larki, S, Alborzi, A, Bahramnejad, K and Asadi, Z (2023) The occurrence of the strongylid nematodes, Kalicephalus viparae viparae (nematoda: Diaphanocephalidae), in viper snakes, Macrovipera lebetina (Reptilia: Viperidae), Southwestern Iran. Archives of Razi Institute, 78(2), 611–618. https://doi.org/10.22092/ari.2022.359446.2418Google ScholarPubMed
Liu, W, Wang, T, Liu, XS, Tan, L, Liu, Y and Liu, YS (2019) Molecular identification of Kalicephalus isolated from snakes in Hunan province, subtropical China. Tropical biomedicine 36(1), 289–296. https://doi.org/10.1016/j.ympev.2006.01.003Google ScholarPubMed
Martins, M and Oliveira, ME (1998) Natural history of snakes in forests of the Manaus Region, central Amazonia, Brazil. Herpetological Natural History 6(2), 78–150.Google Scholar
Miller, MA, Pfeifer, W, Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees” in Proceedings of the Gateway computing environments workshop(GCE), November 2010. New Orleans, LAGoogle Scholar
Nogueira, CC, Argôlo, AJ, Arzamendia, V, Azevedo, JÁ, Barbo, FE; Bérnils, RS et al. (2019) Atlas of Brazilian snakes: Verified point-locality maps to mitigate the Wallacean shortfall in a megadiverse snake fauna. South American Journal of Herpetology 14(1), 1–274. https://doi.org/10.2994/SAJH-D-19-00120.1CrossRefGoogle Scholar
Oliveira, ME, Martins, M (2001) When and where to find a pitviper: activity patterns and habitat use of the lancehead, Bothrops atrox, in Central Amazonia, Brazil. Herpetological Natural History 8(2), 101–110.Google Scholar
Pardal, PPDO, Souza, SM, Monteiro, MRCC, Fan, HW, Cardoso, JLC, França, FOS, … e Warrell, DA (2004) Clinical trial of two antivenoms for the treatment of Bothrops and Lachesis bites in the north eastern Amazon region of Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 98(1), 28–42.10.1016/S0035-9203(03)00005-1CrossRefGoogle ScholarPubMed
Pereira, FB, Ferreira, VL, Tomas, WM, Elisei, C, Paiva, F and Tavares, LER (2018). Diaphanocephalus galeatus (Nematoda: Diaphanocephalidae), a poorly known parasite of lizards: redescription, firstgenetic characterization and a revision of its congeners from Brazil. Journal of Helminthology 93(5), 629–635. https://doi.org/10.1017/S0022149X18000597CrossRefGoogle Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25(7), 1253–1256. https://doi.org/10.1093/molbev/msn083CrossRefGoogle ScholarPubMed
Rambaut, A (2009) Molecular evolution, phylogenetics and epidemiology: Fig-Tree. Available at http://tree.bio.ed.ac.uk/software/figtree/.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574. https://doi.org/10.1093/bioinformatics/btg180CrossRefGoogle ScholarPubMed
Schad, GA (1956) Studies on the genus Kalicephalus (Nematoda: Diaphanocephalidae): I. On the life histories of the North American species K. parvus, K. agkistrodontis, and K. rectiphilus. Canadian Journal of Zoology 34(5), 425–452. https://doi.org/10.1139/z56-047CrossRefGoogle Scholar
Schad, GA (1962) Studies on the genus Kalicephalus (Nematoda: Diaphanocephalidae): II. A taxonomic revision of the genus Kalicephalus Molin, 1861. Canadian Journal of Zoology 40(6), 1035–1165. https://doi.org/10.1139/z62-090CrossRefGoogle Scholar
Siva, AMD, Monteiro, WM and Bernarde, PS (2019) Popular names for bushmaster (Lachesis muta) and lancehead (Bothrops atrox) snakes in the Alto Juruá region: repercussions for clinical-epidemiological diagnosis and surveillance. Revista da Sociedade Brasileira de Medicina Tropical 52. https://doi.org/10.1590/0037-8682-0140-2018CrossRefGoogle ScholarPubMed
Zhang, H, Zhang, S and Zhang, L (2011) Two species of the genus Kalicephalus Molin, 1861 (Nematoda, Diaphanocephaloidea) from the water monitor, Varanus salvator (Laurenti, 1768) in Guangdong Province, China. Acta Parasitologica 56(1), 48–53. https://doi.org/10.2478/s11686-011-0012-3CrossRefGoogle Scholar
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