Abstract
Parasites are part of the natural processes that help regulate populations and maintain ecosystems balanced. There is a growing recognition of parasites as important factors in the conservation of species, mainly those vulnerable to extinction in a changing environment. Bears are good biological models for monitoring infectious agents in wildlife, given their life cycle, broad home range, and severity of interactions with humans and their domestic animals as a result of their behavioral plasticity, intelligence, and omnivorous food habits. In the Andean region, the only bear species listed as vulnerable is the Tremarctos ornatus. To determine the sampling gap and prioritize the approach for understanding parasite diversity in bears, I performed a systematic review and metanalysis of the documented parasites of bears across the world and discussed the possibility of the parasites recorded in these other species being present in the T. ornatus in the Andean region, specifically Colombia. In 283 relevant references, 647 records were found of 189 parasites in 37 countries. Of the bears with parasites recorded, Ursus americanus had the most numerous and complete records. The tropical species H. malayanus, M. ursinus, and T. ornatus showed the smallest parasite diversity and unseen species estimate, despite being the region where the greatest diversity of parasites was expected. Of interest are around 80 parasites that have been recorded in seven non-Colombian bear species but are documented in other species in this country.References
Aguirre AA, Ostfeld RS, Tabor GM, House C, Pearl MC. Conservation medicine: Ecological health in practice. Oxford University Press; 2002.
Wisely SM, Howard J, Williams SA, Bain O, Santymire RM, Bardsley KD, et al. An unidentified filarial species and its impact on fitness in wild populations of the black-footed ferret (Mustela nigripes). J Wildl Dis. 2008;44(1):53-64. https://doi.org/10.7589/0090-3558-44.1.53
Smith KF, Acevedo‐Whitehouse K, Pedersen AB. The role of infectious diseases in biological conservation. Anim Conserv. 2009;12(1):1-12. https://doi.org/10.1111/j.1469-1795.2008.00228.x
Smith KF, Sax DF, Lafferty KD. Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol. 2006;20(5):1349-57. https://doi.org/10.1111/j.1523-1739.2006.00524.x
Zhang L, Yang X, Wu H, Gu X, Hu Y, Wei F. The parasites of giant pandas: Individual-based measurement in wild animals. J Wildl Dis. 2011;47(1):164-71. https://doi.org/10.7589/0090-3558-47.1.164
Patz J, Githeko A, McCarty J, Hussein S, Confalonieri U, De Wet N. Climate change and infectious diseases. In: McMichael, A. J, Campbell-Lendrum, D. H, Corvalán, C. F, Ebi, K. L, Githeko, A. K, Scheraga, J. D, Woodward, A, editors. Climate Change and Human Health. Risks and Responses. Geneva: World Health Organization; 2003. p. 103-32.
Brena P, Gauthier D, Humeau A, Baurier F, Dej F, Lemberger K, et al. How Can Computer Tools Improve Early Warnings for Wildlife Diseases? In: Sèdes, F, editor. How information systems can help in alarm/alert detection. Elsevier; 2018. p. 241-56. https://doi.org/10.1016/B978-1-78548-302-8.50009-5
Ujvari B, Belov K. Major histocompatibility complex (MHC) markers in conservation biology. Int J Mol Sci. 2011;12(8):5168-86. https://doi.org/10.3390/ijms12085168
García Marín JF, Royo LJ, Oleaga A, Gayo E, Alarcia O, Pinto D, et al. Canine adenovirus type 1 (CA dV‐1) in free‐ranging European brown bear (Ursus arctos arctos): A threat for Cantabrian population? Transbound Emerg Dis. 2018;65(6):2049-56. https://doi.org/10.1111/tbed.13013
Mackenstedt U, Jenkins D, Romig T. The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. Int J Parasitol Parasites Wildl. 2015;4(1):71-9. https://doi.org/10.1016/j.ijppaw.2015.01.006
Monsalve-Buriticá S. Enfermedades emergentes y reemergentes de origen viral o bacteriano en Colombia. Medellín: Fondo Editor Biogénesis; 2019. p. 49-62.
McCullough DR. Behavior, bears, and humans. Wildl Soc Bull; 1982;10(1):27-33. https://www.jstor.org/stable/3781798
Gilbert B. Behavioral plasticity and bear-human conflicts. Paper presented at: Bear-people conflicts. Proceedings of a Symposium on Management Strategies; 1989 Jan. Yellowknife, Canada.
Sasmal I, Gould NP, Schuler KL, Chang YF, Thachil A, Strules J, et al. Leptospirosis in urban and suburban american black bears (ursus americanus) in Western North Carolina, USA. J Wildl Dis. 2019;55(1):74-83. https://doi.org/10.7589/2017-10-263
Dubey J, Jones J. Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol. 2008;38(11):1257-78. https://doi.org/10.1016/j.ijpara.2008.03.007
Baruch-Mordo S, Wilson KR, Lewis DL, Broderick J, Mao JS, Breck SW. Stochasticity in natural forage production affects use of urban areas by black bears: Implications to management of human-bear conflicts. PloS One. 2014;9(1):e85122. https://doi.org/10.1371/journal.pone.0085122
Bronson E, Spiker H, Driscoll CP. Serosurvey for selected pathogens in free-ranging American black bears (Ursus americanus) in Maryland, USA. J Wildl Dis. 2014;50(4):829-36. https://doi.org/10.7589/2013-07-155
Elbroch LM, Lendrum PE, Allen ML, Wittmer HU. Nowhere to hide: Pumas, black bears, and competition refuges. Behav Ecol. 2015;26(1):247-54. https://doi.org/10.1093/beheco/aru189
Lesmerises R, Rebouillat L, Dussault C, St-Laurent MH. Linking GPS telemetry surveys and scat analyses helps explain variability in black bear foraging strategies. PLoS One. 2015;10(7):e0129857. https://doi.org/10.1371/journal.pone.0129857
Kindschuh SR, Cain III JW, Daniel D, Peyton MA. Efficacy of GPS cluster analysis for predicting carnivory sites of a wide‐ranging omnivore: The American black bear. Ecosphere. 2016;7(10):e01513. https://doi.org/10.1002/ecs2.1513
Westmoreland LS, Stoskopf MK, Maggi RG. Prevalence of Anaplasma phagocytophilum in North Carolina eastern black bears (Ursus americanus). J Wildl Dis. 2016;52(4):968-70. https://doi.org/10.7589/2016-02-036
Borka-Vitális L, Domokos C, Földvári G, Majoros G. Endoparasites of brown bears in Eastern Transylvania, Romania. Ursus. 2017;28(1):20-30. https://doi.org/10.2192/URSU-D-16-00015.1
Wu J, Han JQ, Shi LQ, Zou Y, Li Z, Yang JF, et al. Prevalence, genotypes, and risk factors of Enterocytozoon bieneusi in Asiatic black bear (Ursus thibetanus) in Yunnan Province, Southwestern China. Parasitol Res. 2018;117(4):1139-45. https://doi.org/10.1007/s00436-018-5791-0
Stephenson N, Higley JM, Sajecki JL, Chomel BB, Brown RN, Foley JE. Demographic characteristics and infectious diseases of a population of American black bears in Humboldt County, California. Vector-Borne Zoonotic Dis. 2015;15(2):116-23. https://doi.org/10.1089/vbz.2014.1671
Peña-Quistial MG, Benavides-Montaño JA, Duque NJR, Benavides-Montaño GA. Prevalence and associated risk factors of Intestinal parasites in rural high-mountain communities of the Valle del Cauca—Colombia. PLoS Negl Trop Dis. 2020;14(10):e0008734. https://doi.org/10.1371/journal.pntd.0008734
Schwab C, Cristescu B, Northrup JM, Stenhouse GB, Gänzle M. Diet and environment shape fecal bacterial microbiota composition and enteric pathogen load of grizzly bears. PLoS One. 2011;6(12):e27905. https://doi.org/10.1371/journal.pone.0027905
Ishibashi Y, Oi T, Arimoto I, Fujii T, Mamiya K, Nishi N, et al. Loss of allelic diversity in the MHC class II DQB gene in western populations of the Japanese black bear Ursus thibetanus japonicus. Conserv Genet. 2017;18(2):247-60. https://doi.org/10.1007/s10592-016-0897-3
Goldstein I, Paisley S, Wallace R, Jorgenson JP, Cuesta F, Castellanos A. Andean bear–livestock conflicts: a review. Ursus. 2006;17(1):8–15. https://doi.org/10.2192/1537-6176(2006)17[8:ABCAR]2.0.CO;2
Bard SM, Cain III JW. Pathogen prevalance in American black bears (Ursus americanus amblyceps) of the Jemez Mountains, New Mexico, USA. J Wildl Dis. 2019;55(4):745-54. https://doi.org/10.7589/2018-12-286
Velez-Liendo X, García-Rangel S. The IUCN Red List of Threatened Species 2017: e.T22066A123792952. 2018 [cited 2022 Nov 21]. Tremarctos ornatus. Available from: https://www.iucnredlist.org/species/22066/123792952
Peyton B. Spectacled bear conservation action plan. Bears: Status Survey and Conservation Action Plan. IUCN: 1999. p. 157-64.
Goldstein IR. Andean bear-cattle interactions and tree nest use in Bolivia and Venezuela. Ursus. 2002;13:369-72. https://www.jstor.org/stable/3873218
Kattan G, Hernández OL, Goldstein I, Rojas V, Murillo O, Gómez C, et al. Range fragmentation in the spectacled bear Tremarctos ornatus in the northern Andes. Oryx. 2004;38(2):155-63. https://doi.org/10.1017/S0030605304000298
Jorgenson JP, Sandoval-A S. Andean bear management needs and interactions with humans in Colombia. Ursus. 2005;16(1):108-16. https://doi.org/10.2192/1537-6176(2005)016[0108:ABMNAI]2.0.CO;2
Parra-Romero A, Zamudio-López J, Camargo-Cárdenas JE, Palacios-Medina CR, Torres L, Castro E, et al. Ocupación del oso andino (Tremarctos ornatus) en la región centro-norte de la Cordillera Oriental de Colombia [Internet]. PNN de Colombia, CAR Cundinamarca, Corpoboyacá, Corporinoquía, Corpochivor, Cormacarena, Corpoguavio, ABCA y WCS; 2019. 32 p.
King JS, Jenkins DJ, Ellis JT, Fleming P, Windsor PA, Šlapeta J. Implications of wild dog ecology on the sylvatic and domestic life cycle of Neospora caninum in Australia. Vet J. 2011;188(1):24-33. https://doi.org/10.1016/j.tvjl.2010.03.002
Palmer MW. Estimating species richness: The second-order jackknife reconsidered. Ecol Durh. 1991;72(4):1512-3. https://doi.org/10.2307/1941127
Colwell RK, Coddington JA. Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci. 1994;345(1311):101-18. https://doi.org/10.1098/rstb.1994.0091
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, Simpson GL, Solymos P, Stevens MH, Wagner H. Package ‘vegan’. Community Ecology Package, version 2. The comprehensive R network (CRAN).[Google Scholar]. 2013.
Diamond J. Sociedades comparadas: Un pequeño libro sobre grandes temas. Bogotá; Debate: 2016.
Navarro M. D, Chávez V. A, Pinedo V. R, Muñoz D. K. Factores de Riesgo Asociados a la Seroprevalencia de Toxoplasma gondii en Mamíferos del Orden Carnivora y Primates Mantenidos en Cautiverio. Rev Investig Vet Perú [Internet]. 2015 Dec 31 [cited 2023 Aug 14];26(3):497. https://doi.org/10.15381/rivep.v26i3.11175
Mata AP, Pérez HG, Parra JG. Morphological molecular description of Baylisascaris venezuelensis, n. sp. from a natural infection in the South American spectacled bear Tremarctos ornatus Cuvier, 1825 in Venezuela. Neotrop Helminthol. 2016;10:85-103.
Oniki-Willis Y, Willis EO. Tick (Acarina) diversity from South American birds and mammals. Atual Ornitológicas. 2018;(206).
Zárate Rodriguez PT, Collazos-Escobar LF, Benavides-Montaño JA. Endoparasites Infecting Domestic Animals and Spectacled Bears (Tremarctos ornatus) in the Rural High Mountains of Colombia. Vet Sci [Internet]. 2022 Sep 29 [cited 2023 Aug 14];9(10):537. https://doi.org/10.3390/vetsci9100537
Quintero LR, Pulido-Villamarín A, Parra-Romero Á, Castañeda-Salazar R, Pérez-Torres J, Vela-Vargas IM. Andean bear gastrointestinal parasites in Chingaza Massif, Colombia. Ursus [Internet]. 2023 Jul 12 [cited 2023 Aug 14];2023(34e4). https://doi.org/10.2192/URSUS-D21-00020.1
Figueroa J. New records of parasites in free-ranging Andean bears from Peru. Ursus [Internet]. 2015 May [cited 2022 Nov 21];26(1):21-7. https://doi.org/10.2192/URSUS-D-14-00034.1
Cruz Hurtado SSM, Muñoz Huamaní M. Identificación de parásitos gastrointestinales de carnívoros en cautiverio criados en el centro recreacional municipal del Cerrito de la Libertad de Huancayo [dissertation]. [Huancayo] Universidad Peruana de los Andes; 2016. 90 p. Available from: https://hdl.handle.net/20.500.12848/114
Chica Cardenas LA. Estimating the andean bear diet through DNA metabarcoding and its relationships to the gut microbiome [Internet]. Universidad de los Andes; 2021. Available from: https://repositorio.uniandes.edu.co/handle/1992/58061
Longmire JL, Maltbie M, Baker RJ. Use of" lysis buffer" in DNA isolation and its implication for museum collections. 1997; (163). https://doi.org/10.5962/bhl.title.143318
Wultsch C, Waits LP, Hallerman EM, Kelly MJ. Optimizing collection methods for noninvasive genetic sampling of neotropical felids. Wildl Soc Bull. 2015;39(2):403-12. https://doi.org/10.1002/wsb.540
Semblante GU, Phan HV, Hai FI, Xu ZQ, Price WE, Nghiem LD. The role of microbial diversity and composition in minimizing sludge production in the oxic-settling-anoxic process. Sci Total Environ [Internet]. 2017 Dec [cited 2023 Aug 14];607-608:558-67. https://doi.org/10.1016/j.scitotenv.2017.06.253
Francis EK, Šlapeta J. A new diagnostic approach to fast-track and increase the accessibility of gastrointestinal nematode identification from faeces: FECPAKG2 egg nemabiome metabarcoding. Int J Parasitol [Internet]. 2022 May [cited 2023 Aug 14];52(6):331-42. https://doi.org/10.1016/j.ijpara.2022.01.002
Stensvold CR, Jirků-Pomajbíková K, Tams KW, Jokelainen P, Berg RPKD, Marving E, et al. Parasitic Intestinal Protists of Zoonotic Relevance Detected in Pigs by Metabarcoding and Real-Time PCR. Microorganisms [Internet]. 2021 May 31 [cited 2023 Aug 14];9(6):1189. https://doi.org/10.3390/microorganisms9061189
Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol [Internet]. 2019 Nov 28 [cited 2023 Aug 14];20(1):257. https://doi.org/10.1186/s13059-019-1891-0
Han BA, Kramer AM, Drake JM. Global Patterns of Zoonotic Disease in Mammals. Trends Parasitol [Internet]. 2016 Jul [cited 2023 Aug 14];32(7):565-77. https://doi.org/10.1016/j.pt.2016.04.007
Shaheen MNF. The concept of one health applied to the problem of zoonotic diseases. Rev Med Virol [Internet]. 2022 Jul [cited 2023 Aug 14];32(4). https://doi.org/10.1002/rmv.2326
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Copyright (c) 2024 Revista de Medicina Veterinaria
Keywords
infectious agents
Tremarctos ornatus
Ursids