Morphological and molecular identification of the hard ticks parasitizing Tremarctos ornatus (Carnivora: Ursidae) from paramo of Ecuador

Year 2023, , 45 - 51, 31.07.2023

Sandra Enríquez , María L. Félix Armando Castellanos Sergio Bermudez Castıllero , José M. Venzal

https://doi.org/10.47121/acarolstud.1261833

Cited By: 2

Abstract

The Andean bear or spectacled bear, Tremarctos ornatus (Cuvier), inhabits the Andes and is considered an endangered species due to anthropogenic factors. The aim of this study was to identify the tick species parasitizing the Andean bears in the evergreen shrubland and paramo grassland ecosystem in the Andes Mountain Range of Ecuador. Twenty-six ticks were removed from five Andean bears and morphologically identified as Amblyomma multipunctum Neumann, Ixodes boliviensis Neumann and Ixodes montoyanus Cooley. One specimen of each species was also molecularly analyzed and confirmed by BLAST. This study confirms the presence of I. boliviensis parasitizing T. ornatus and adds new records of A. multipunctum and I. montoyanus in its distribution. The parasite-host relationships are new in all cases for Ecuador.

Keywords

Ixodidae, Amblyomma, Ixodes, Andean bear, paramo, Ecuador

Supporting Institution

Andean Bear Foundation (ABF) and ZooConservation Outreach Group, USA funds supported the fieldwork.

Thanks

To Melchor Ascanta, Rodrigo Ascanta, David Jackson, Alandy Torres, Flavio Torres, Daniel Hilliard of ZCOG, Jorge Brito of INABIO, Edgar Martínez, and Raúl Martínez for their support in the capture, management, and release of the captured Andean Bears. To The Andean Bear Foundation (ABF), for working to conserve the Spectacled/Andean Bear. To Zoo Conservation Outreach Group (ZCOG) for assisting Latin American wildlife and habitat conservation efforts. To the Ministerio del Ambiente y Agua del Ecuador for supporting research projects via Collection Permits.

References

• Aguilar-Domínguez, M., Moo-Llanes, D.A., Sánchez-Montes, S., Becker, I., Feria-Arroyo, T.P., de León, A.P. and Romero-Salas, D. 2021. Potential distribution of Amblyomma mixtum (Koch, 1844) in climate change scenarios in the Americas. Ticks and Tick-borne Diseases, 12 (6): 101812. doi.org/10.1016/j.ttbdis.2021.101812
• Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215 (3): 403-410. doi: 10.1016/S0022-2836(05)80360-2
• Anonymous. 1998. Disease vector ecology profile: Colombia. Defense Pest Management Information Analysis Center, Armed Forces Pest Management Board, Forest Glen Section, Walter Reed Army Medical Center, Washington, DC, USA, 89 pp.
• Apanaskevich, D.A. and Bermúdez, S.E. 2017. Description of a new species of Ixodes Latreille, 1795 (Acari: Ixodidae) and redescription of I. lasallei Méndez & Ortiz, 1958, parasites of agoutis and pacas (Rodentia: Dasyproctidae, Cuniculidae) in Central and South America. Systematic Parasitology, 94: 463-475. doi 10.1007/s11230-017-9718-4
• Apanaskevich, D.A., Domínguez, L.G., Torres, S.S., Bernal, J.A., Montenegro, V.M. and Bermúdez, S.E. 2017. First description of the male and redescription of the female of Ixodes tapirus Kohls, 1956 (Acari: Ixodidae), a parasite of tapirs (Perissodactyla: Tapiridae) from the mountains of Colombia, Costa Rica, and Panama. Systematic Parasitology, 94 (3): 413-422. doi: 10.1007/s11230-017-9706-8
• Bermúdez, S.E., Félix, M.L., Domínguez, L., Kadoch, N., Muñoz-Leal, S. and Venzal, J.M. 2021. Molecular screening for tick-borne bacteria and hematozoa in Ixodes cf. boliviensis and Ixodes tapirus (Ixodida: Ixodidae) from western highlands of Panama. Current Research in Parasitology & Vector-Borne Diseases, 1: 100034. doi.org/10.1016/j.crpvbd.2021.100034
• Black, W.C. 4th. and Piesman, J. 1994. Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proceedings of the National Academy of Sciences, 91 (21): 10034-10038. doi: 10.1073/pnas.91.21.10034
• Carvajal, L.V. and Castellanos, A. 2021. Nuevos registros de ectoparásitos (Ixodidae) sobre oso Andino. Boletín Técnico, Serie Zoológica, 15 (16): 10-17. [In Spanish]
• Castellanos, A. 2010. Guía para la rehabilitación, liberación y seguimiento de osos Andinos. Ministerio del Ambiente, Quito, Ecuador, 34 pp.[In Spanish]
• Castellanos, A., dos Santos, C.C., Álvarez, W., Arias, L. and Viteri, V. 2018. Manual y protocolo de captura, inmovilización, marcaje y migración de datos satelitales de tapires amazónicos (Tapirus terrestris) y jaguares (Panthera onca) en el Parque Nacional Yasuní. Desarrollo e implementación piloto del Sistema Nacional de Monitoreo de la Biodiversidad SINMBIO, Ministerio del Ambiente, KFW, IKIAM, ECOCIENCIA, Quito, Ecuador, 70 pp. [In Spanish]
• Castellanos-Peñafiel, A.X., Brito, J. and Castellanos-Insuasti, F.X. 2021. Tapirus pinchaque in Southwestern Ecuador. Boletín Técnico, Serie Zoológica, 15 (16): 1-4.
• Cooley, R.A. 1944. Ixodes montoyanus (Ixodidae) a new tick from Colombia. Pan American Sanitary Bureau Bulletin, 23 (9): 804-806.
• Díaz, N.M., Méndez, G.S., Grijalva, C.J., Walden, H.S., Cruz, M., Aragón, E. and Hernández, J.A. 2016. Dog overpopulation and burden of exposure to canine distemper virus and other pathogens on Santa Cruz Island, Galapagos. Preventive Veterinary Medicine, 123: 128-137. doi: 10.1016/j.prevetmed.2015.11.016
• Enríquez, S., Guerrero, R., Arrivillaga‑Henríquez, J., Araujo, P., Villacrés, E., Enríquez, A. and Benítez‑Ortíz, W. 2020. New records of ticks of genus Amblyomma Koch, 1844 (Acari: Ixodidae) for Ecuador. Acta Parasitologica, 65 (2): 430-440. doi: 10.2478/s11686-020-00173-7
• Estrada-Peña, A., Tarragona, E.L., Vesco, U., Meneghi, D.D., Mastropaolo, M., Mangold, A.J., Guglielmone, A.A. and Nava, S. 2014. Divergent environmental preferences and areas of sympatry of tick species in the Amblyomma cajennense complex (Ixodidae). International Journal for Parasitology, 44 (14): 1081-1089. doi: 10.1016/j.ijpara.2014.08.007
• Galeas, R., Guevara, J.E., Medina-Torres, B., Chinchero, M.Á. and Herrera, X. (Eds). 2013. Sistema de clasificación de ecosistemas del Ecuador Continental. Subsecretaría de Patrimonio Natural Proyecto mapa de vegetacion. Ministerio del Ambiente, Ecuador, 232 pp. [In Spanish]
• Gioia, G.V., Vinueza, R.L., Marsot, M., Devillers, E., Cruz, M., Petit, E., Boulouis, H.J., Moutailler, S., Monroy, F., Coello, M.A., Gondard, M., Bournez, L., Haddad, N. and Zanella, G. 2018. Bovine anaplasmosis and tick-borne pathogens in cattle of the Galapagos Islands. Transboundary and Emerging Diseases, 65 (5): 1262-1271. doi: 10.1111/tbed.12866
• Guglielmone, A.A., Petney, T.N. and Robbins, R.G. 2020. Ixodidae (Acari: Ixodoidea): descriptions and redescriptions of all known species from 1758 to December 31, 2019. Zootaxa, 4871 (1): 1-322. doi: 10.11646/zootaxa.4871.1.1
• Guglielmone, A.A., Nava, S. and Robbins, R.G. 2021. Neotropical Hard Ticks (Acari: Ixodida: Ixodidae): A critical analysis of their taxonomy, distribution, and host relationships. Springer International Publishing, Cham, Switzerland, 486 pp. doi: 10.1007/978-3-030-72353-8
• Guglielmone, A.A., Nava, S. and Robbins, R.G. 2023. Geographic distribution of the hard ticks (Acari: Ixodida: Ixodidae) of the world by countries and territories. Zootaxa, 5251 (1): 1-274. doi: 10.11646/zootaxa.5251.1.1
• IUCN. 2022. The IUCN Red list of threatened species. Version 2022-2. Available from https://www.iucnredlist.org/search?query=Tremarctos%20ornatus&searchType=species (Last accessed: 25 Nov. 2022).
• Keirans, J.E. 1973. Ixodes (I.) montoyanus Cooley (Acarina: Ixodidae): First description of the male and immature stages, with records from deer in Colombia and Venezuela. Journal of Medical Entomology, 10 (3): 249-254. doi: 10.1093/jmedent/10.3.249
• Kumar, S., Stecher, G. and Tamura, K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7): 1870-1874. doi: 10.1093/molbev/msw054
• Labruna, M.B., Martins, T., Nunes, P., Costa, B., Portero, F. and Venzal, J.M. 2013. New records of Amblyomma multipunctum and Amblyomma napoense from Ecuador, with description of A. multipunctum nymph. Journal of Parasitology, 99 (6): 973-977. doi: 10.1645/13-254.1
• Labruna, M.B., Onofrio, V.C., Barros-Battesti, D.M., Gianizella, S.L., Venzal, J.M. and Guglielmone, A.A. 2020. Synonymy of Ixodes aragaoi with Ixodes fuscipes, and reinstatement of Ixodes spinosus (Acari: Ixodidae). Ticks and Tick-borne Diseases, 11 (2): 101349. doi: 10.1016/j.ttbdis.2019.101349
• Maya-Delgado, A., Maddere, M., Benítez-Ortíz, W., Saegerman, C., Berkvens, D. and Ron-Garrido, L. 2020. Molecular screening of cattle ticks, tick-borne pathogens and amitraz resistance in ticks of Santo Domingo de los Tsáchilas province in Ecuador. Ticks and Tick-borne Diseases, 11 (5): 101492. doi: 10.1016/j.ttbdis.2020.101492
• Nava, S., Beati, L., Labruna, M.B., Cáceres, A.G., Mangold, A.J. and Guglielmone, A.A. 2014. Reassessment of the taxonomic status of Amblyomma cajennense (Fabricius, 1787) with the description of three new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp. and Amblyomma patinoi n. sp., and reinstatement of Amblyomma mixtum and Amblyomma sculptum (Ixodida: Ixodidae). Ticks and Tick-borne Diseases, 5 (3): 252-276. doi: 10.1016/j.ttbdis.2013.11.004
• Onofrio, V.C., Labruna, M.B., Pinter, A., Giacomin, F.G. and Barros-Battesti, D.M. 2006a. Comentários e chaves para as espécies do genero Amblyomma. In: Carrapatos de Importância Médico-Veterinária da Região Neotropical. Um guia ilustrado para identificação de espécies. Barros-Battesti, D.M., Arzua, M. and Bechara, G.H. (Eds). São Paulo, Vox/ICTTD-3, Butantan, Brasil, 53-113. [In Portuguese]
• Onofrio, V.C., Labruna, M.B. and Barros-Battesti, D.M. 2006b. Comentários e chaves para as espécies do genero Ixodes. In: Carrapatos de Importância Médico-Veterinária da Região Neotropical. Um guia ilustrado para identificação de espécies. Barros-Battesti, D.M., Arzua, M. and Bechara, G.H. (Eds). São Paulo, Vox/ICTTD-3, Butantan, Brasil, 41-51. [In Portuguese]
• Onofrio, V.C., Guglielmone, A.A., Barros-Battesti, D.M., Gianizella, S.L., Marcili, A., Quadros, R.M., Marques, S. and Labruna, M.B. 2020. Description of a new species of Ixodes (Acari: Ixodidae) and first report of Ixodes lasallei and Ixodes bocatorensis in Brazil, Ticks and Tick-borne Diseases, 11 (4): 101423. doi: 10.1016/j.ttbdis.2020.101423
• Paucar, V., Pérez-Otáñez, X., Rodríguez-Hidalgo, R., Perez, C., Cepeda-Bastidas, D., Grijalva, J., Enríquez, S., Arciniegas-Ortega, S., Vanwambeke, S.O., Ron-Garrido, L. and Saegerman, C. 2022. The associated decision and management factors on cattle tick level of infestation in two tropical areas of Ecuador. Pathogens, 11 (4): 403. doi: 10.3390/pathogens11040403
• Pesquera, C., Portillo, A., Palomar, A.M. and Oteo, J.A. 2015. Investigation of tick-borne bacteria (Rickettsia spp., Anaplasma spp., Ehrlichia spp. and Borrelia spp.) in ticks collected from Andean tapirs, cattle and vegetation from a protected area in Ecuador. Parasites & Vectors, 8: 46. doi: 10.1186/s13071-015-0662-3
• Pilatasig, A.L. 2022. First report of parasitism of Ixodes luciae Sénevet, 1940 (Acari: Ixodidae) in two species of bats Sturnira giannae and Glossophaga soricina (Chiroptera: Phyllostomidae). Revista Argentina de Parasitología, 11 (2): 7-10. [In Spanish]
• Polanco-Echeverry, D.N. and Ríos-Osorio, L.A. 2016. Biological and ecological aspects of hard ticks. Ciencia y Tecnología Agropecuaria, 17 (1): 81-95. [In Spanish] doi: 10.21930/rcta.vol17_num1_art:463
• Rodríguez-Hidalgo, R., Pérez-Otáñez, X., Garcés-Carrera, S., Vanwambeke, S.O., Madder, M. and Benítez-Ortiz, W. 2017. The current status of resistance to alpha-cypermethrin, ivermectin, and amitraz of the cattle tick (Rhipicephalus microplus) in Ecuador. PLoS ONE, 12 (4): e0174652. doi: 10.1371/journal.pone.0174652
• Sandoval Guillén, P. and Yánez Moretta, P. 2019. Biological and ecological aspects of the spectacled bear (Tremarctos ornatus, Ursidae) in the Ecuadorean Andean zone and conservation perspectives under the Landscape Species approach. La Granja: Revista de Ciencias de la Vida, 30 (2): 19-27. [In Spanish] doi: 10.17163/lgr.n30.2019.02
• Tirira, D. 2017. A field guide to the mammals of Ecuador. Editorial Murciélago Blanco, Quito, Ecuador, 600 pp.