MORPHOLOGICAL AND GENETIC CHARACTERIZATION OF NEMATODES OF THE OPOSSUM Didelphis albiventris AND THE ARMADILLO Dasypus novemcinctus FROM SERRA DA CAPIVARA NATIONAL PARK
DOI:
https://doi.org/10.4257/oeco.2019.2302.10Keywords:
Aspidoderidae, genetics, helminths, scanning electron microscopy, Trichostrongylidae, protected areasAbstract
Serra da Capivara National Park (SCNP) in Northeast Brazil has the largest concentration of prehistoric sites in the Americas where studies of coprolites of ancestral parasitic fauna reported the presence of morphotypes of nematode eggs identified as Aspidoderidae and Trichostrongyloidea from dasypodid hosts. Among the current mammals inhabiting the park, the opossum Didelphis albiventris and the armadillo Dasypus novemcinctus were found roadkill in the nearby area. The aim of this work was to perform an integrative taxonomic analysis of adult nematode parasites of D. albiventris (N = 3) and D. novemcinctus (N = 2) found roadkill in the SCNP using morphological, ultrastructural and genetic approaches. The nematodes studied included Aspidodera raillieti and Aspidodera subulata (Aspidoderidae) collected from D. albiventris, and Aspidodera binansata, Aspidodera vazi (Aspidoderidae) and Hadrostrongylus speciosum (Trichostrongylidae) from D. novemcinctus. A new geographic locality of four species of Aspidoderidae and one Trichostrongylidae species are reported with new ultrastructural data using scanning electron microscopy of A. binansata and A. vazi. New genetic data of aspidoderids include sequences of partial 18S rRNA (SSU) and partial 28S rRNA (LSU) genes of A. raillieti, the first sequence of 16S rRNA of A. vazi and additional sequences of mitochondrial DNA cytochrome c-oxidase subunit 1, internal transcribed spacer 1, 2 and 5.8S rRNA gene of A. raillieti. These are the first partial sequences of 18S rRNA (SSU) and 28S rRNA (LSU) genes of species of the family Aspidoderidae, linked to a vouchered specimen.
References
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
Araujo, A., Rangel, A., Ferreira, L. F. R., 1993. Climatic change in northeastern Brazil: paleoparasitological data. Memórias do Instituto Oswaldo Cruz (Impresso), RIO DE JANEIRO, v. 88, n.4, p. 577-579, 1993.
Araújo, A. J. G., Pessis, A. A.-M., Guérin, C., Dias, C. M. M., Alves, C., & La Salvia, E. S. 1998. Parque Nacional Serra da Capivara. São Paulo, Tylaser Desenvolvimento Ed. Ltda., 94p.
Brandão, M. L., Chame, M., Cordeiro, J. L. P., & Chaves, S. D. M. 2009. Diversidade de helmintos intestinais em mamíferos silvestres e domésticos na Caatinga do Parque Nacional Serra da Capivara, sudeste do Piauí, Brasil. Revista Brasileira de Parasitologia Veterinária, 18(S1), 19–28. DOI: 10.4322/rbpv.018e1004
Blouin, M. S., Yowell, C. A., Courtney, C. H., & Dame, J. B. 1998. Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology Evolution, 15(12), 1719–1727.
Blouin, M. S. 2002. Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal of Parasitology, 32(5), 527–531.
Cavalcante, P. H. O., Moravec, F. & Santos, C. P. 2018. The philometrid nematode Philometroides acreanensis n. sp. from the stomach wall of the catfish Pimelodus blochii in north-western Brazil. Journal of Helminthology, 92, 109–115. DOI: 10.1017/S0022149X1700013X
Chame, M. 2007. Reservatórios de água e implicações na distribuição de mamíferos cinegéticos no semiárido: contribuições à conservação do Parque Nacional Serra da Capivara, sudeste do Piauí, Brasil. Doctoral thesis. Instituto de Biologia da Universidade Federal do Rio de Janeiro. p. 134.
Chagas-Moutinho, V. A., Oliveira-Menezes, A., Cárdenas, M. Q., & Lanfredi, R. M. 2007. Further description of Aspidodera raillieti (Nematoda: Aspidoderidae) from Didelphis marsupialis (Mammalia: Didelphidae) by light and scanning electron microscopy. Parasitology Research, 101, 1331–1336. DOI: 10.1007/s00436-007-0641-5
Chagas-Moutinho, V. A., Sant’anna, V., Oliveira-Menezes, A. & De Souza, W. 2014. New Aspidoderidae species parasite of Didelphis aurita (Mammalia: Didelphidae): A light and scanning electron microscopy approach. Acta Tropica, 130, 162–166. DOI: 10.1016/j.actatropica.2013.10.005
D'amelio, S., Gasser, R., Palm, H., George-Nascimento, M., Zhu, X. Q., & Paggi, L. 2002. SSCPbased identification of members within the Pseudoterranova decipiens complex (Nematoda: Ascaridoidea: Anisakidae) using genetic markers in the internal transcribed spacers of ribosomal DNA. Parasitology, 124(6), 615–623. DOI: 10.1017/S0031182002001579
Ferreira L. F., Araujo A., Confalonieri, U., Chame, M., Gomez, D. C. 1991. Trichuris eggs in animal coprolites dated from 30,000 years ago. Journal Parasitology 77, 491–493.
FUMDHAM - Fundação Museu do Homem Americano. 2016. Accessed on 08 June, 2018, from http://www.fumdham.org.br/#
Gu, X., Zhu, J-Y., Jian, K-L., Wang, B-J., Peng, X-R., Yang, G-Y., Zhong, W. Z-J., & Peng, K-Y. 2015. Absence of population genetic structure in Heterakis gallinarum of chicken from Sichuan, inferred from mitochondrial cytochrome c oxidase subunit I gene. Mitochondrial DNA Part A, 27(5), 3612–3617. DOI: 10.3109/19401736.2015.1079825
Gutiérrez-Gutiérrez, C., Cantalapiedra-Navarrete, C., Montes-Borrego, M., Palomares-Rius, J. E., & Castillo, P. 2013. Molecular phylogeny of the nematode genus Longidorus (Nematoda: Longidoridae) with description of three new species. Zoology Journal Linnean Society, 167, 473–500. DOI: 10.1111/zoj.12019
Hoppe, E. G. L., & Nascimento, A. A. 2007. Natural infection of gastrointestinal nematodes in longnosed armadillos Dasypus novemcinctus Linnaeus, 1758 from Pantanal wetlands, Aquidauana sub-region, Mato Grosso do Sul State, with the description of Hadrostrongylus speciosum n. gen. et n. sp. (Molineidae: Anoplostrongylinae). Veterinary Parasitology, 144(1–2), 87–92. DOI: 10.1016 /j.vetpar.2006.09.028
Jiménez-Ruiz, F. A., Gardner, S. L., Navone, G. T., & Ortí, G. 2012. Four events of host switching in Aspidoderidae (Nematoda) involve convergent lineages of mammals. Journal of Parasitology, 98(6), 1166–1175. DOI: 10.1645/GE-3045.1
Jiménez-Ruiz, F. A., Carreno, R. A., & Gardner, S. L. 2013. Aspidodera kinsellai n. sp. (Nematoda: Heterakoidea) from nine-banded armadillos in Middle America with notes on phylogeny and host-parasite biogeography. Journal of Parasitology, 99(6), 1056–1061. DOI: 10.1645/13-196.1
Jorge, F., Perera, A., Roca, V., Carretero, M. A., Harris, D. J., & Poulin, R. 2014. Evolution of alternative male morphotypes in oxyurid nematodes: a case of convergence? Journal of Evolutionary Biology, 27(8), 1631–1643. DOI: 10.5061/dryad.cb5f3
Jorge, F., Roca, V., Perera, A., Harris, D. J., & Carretero, M. A. 2011. A phylogenetic assessment of the colonisation patterns in Spauligodon atlanticus Astasio-Arbiza et al., 1987 (Nematoda: Oxyurida: Pharyngodonidae), a parasite of lizards of the genus Gallotia Boulenger: no simple answers. Systematic Parasitology, 80(1), 53–66. DOI: 10.1007/s11230-011-9311-1
Klimpel, S., Kleinertz, S., Hanel, R., & Rückert, S. 2007. Genetic variability in Hysterothylacium aduncum, a raphidascarid nematode isolated from sprat (Sprattus sprattus) of different geographical areas of the northeastern Atlantic. Parasitolology Research, 101, 1425–1430. DOI: 10.1007/s00436-007-0662-0
Malysheva, S. V. 2014. A new species of Carnoya Gilson, 1898 (Nematoda: Ransomnematoidea: Carnoyidae) from Sumba Island, Indonesia. Russian Journal of Nematology, 22(2), 157–164.
Malysheva, S. V., Luc, P. V., & Spiridonov, S. E. 2012. Insulanema longispiculum gen. n., sp. n. a new Carnoyidae (Nematoda: Rhigonematomorpha) from Phu Quoc Island, Vietnam. Russian Journal of Nematology, 20(12), 157–166.
Nadler, S. A. 1992. Phylogeny of some ascaridoid nematodes, inferred from comparison of 18S and 28S rRNA sequences. Molecular Biology and Evolution, 9(5), 932–944.
Nadler, S. A., & Hudspeth, D. S. S. 2000. Phylogeny of the Ascaridoidea (Nematode: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. Journal of Parasitology, 86, 380–393.
Nadler, S. A., & Hudspeth, D. S. 1998. Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): implications for morphological evolution and classification. Molecular Phylogenetics and Evolution, 10 (2), 221–236.
Nadler, S. A., Carreno, R. A., Mejía-Madrid, H., Ullberg, J., Pagan, C., Houston, R., & Hugot, J-P. 2007. Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology, 134, 1421–1442. DOI: 10.1017/S0031182007002880
Nylander, J. A. A. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
Okamoto, M., Urushima, H., & Hasegawa, H. 2009. Phylogenetic relationships of rodent pinworms (genus Syphacia) in Japan inferred from 28S rDNA sequences. Parasitology International, 58(4), 330–333. DOI: 10.1016/j.parint.2009.07.001
Prosser, S. W., Velarde-Aguilar, M. G., León-Règagnon, V., & Hebert, P. D. 2013. Advancing nematode barcoding: a primer cocktail for the cytochrome c oxidase subunit I gene from vertebrate parasitic nematodes. Molecular Ecology Resources, 13(6), 1108–1115. DOI: 10.1111/1755-0998.12082
Santos, C. P., Lent, H., & Gomes, D. C. 1990. The genus Aspidodera Railliet and Henry, 1912 (Nematoda: Heterakoidea): revision, new synonyms and key of species. Revista Brasileira de Biologia, 50, 1017–1031.
Sianto, L. 2009. Parasitismo em populações Pré-Colombianas: helmintos de animais em coprólitos de origem humana do Parque Nacional Serra da Capivara, PI, Brasil. Doctoral thesis. Escola Nacional de Saúde Pública Sérgio Arouca. 183 p.
Souza, M. V. D., Sianto, L., Chame, M., Ferreira, L. F., & Araújo, A. 2012. Syphacia sp. (Nematoda: Oxyuridae) in coprolites of Kerodon rupestris Wied, 1820 (Rodentia: Caviidae) from 5,300 years BP in northeastern Brazil. Memórias do Instituto Oswaldo Cruz 107(4), 539–542.
Subbotin, S. A., Stanley, J. D., Ploeg, A. T., Maafi, Z. T., Emmanuel, A. T., Chitambar, J. J., Palomares-Rius, J. E., Castillo, P., & Inserra, R. N. 2015. Characterization of populations of Longidorus orientalis Loof, 1982 (Nematoda: Dorylaimida) from date palm (Phoenix dactylifera L.) in the USA and other countries and incongruence of phylogenies inferred from ITS1 rRNA and coxI genes. Nematology, 17, 459–477. DOI: 10.1163/15685411-00002881
Swofford, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods), 4.0 edn, Sinauer, Sunderland, MA.
Tran, B. T., Ong, A. V., Luc, P. V., & Sato, H. 2016. Morphological and molecular genetic diversity of Strongyluris calotis (Nematoda: Ascaridida: Heterakidae) in South East and East Asian lizards. Parasitology Research, 115(7), 2807–2816. DOI: 10.1007/s00436-016-5030-5
Vicente, J. J. 1966. Revisão da subfamília Aspidoderidae Skrjabi & Shikhobalova, 1947 (Nematoda). Memórias do Instituto Oswaldo Cruz, 64, 131–161.
Vicente, J. J., Rodrigues, H. O., Gomes, D. C., & Pinto, R. M. 1997. Nematóides do Brasil. Parte V. Nematóides de mamíferos. Revista Brasileira Biologia, 14(1), 1–452.
