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Epidemiological approach to nematode polyparasitism occurring in a sympatric wild ruminant multi-host scenario

Published online by Cambridge University Press:  07 June 2021

Tessa Carrau
Affiliation:
Department of Animal Health, Campus de Excelencia Internacional Regional ‘Campus Mare Nostrum’, University of Murcia, 30100 Espinardo, Murcia, Spain
Carlos Martínez-Carrasco
Affiliation:
Department of Animal Health, Campus de Excelencia Internacional Regional ‘Campus Mare Nostrum’, University of Murcia, 30100 Espinardo, Murcia, Spain
María Magdalena Garijo
Affiliation:
Department of Animal Production and Health, Public Veterinarian Health and Food Science and Technology, Veterinary Faculty, Cardenal Herrera-CEU University, CEU Universities, C/ Tirant lo Blanc, 7, 46115 Alfara del Patriarca, Valencia, Spain
Francisco Alonso
Affiliation:
Department of Animal Health, Campus de Excelencia Internacional Regional ‘Campus Mare Nostrum’, University of Murcia, 30100 Espinardo, Murcia, Spain
Luis León Vizcaíno
Affiliation:
Department of Animal Health, Campus de Excelencia Internacional Regional ‘Campus Mare Nostrum’, University of Murcia, 30100 Espinardo, Murcia, Spain
José Herrera-Russert
Affiliation:
Institute for Insect Biotechnology, Justus-Liebig-University, Heinrich-Buff-Ring 26-32, D-35392, Giessen, Germany
Paolo Tizzani*
Affiliation:
Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2–10095 Grugliasco (Torino), Italy
Rocío Ruiz de Ybáñez
Affiliation:
Department of Animal Health, Campus de Excelencia Internacional Regional ‘Campus Mare Nostrum’, University of Murcia, 30100 Espinardo, Murcia, Spain
*
Author for correspondence: Paolo Tizzani, E-mail: [email protected]

Abstract

The epidemiology behind multi-host/multi-parasite systems is particularly interesting to investigate for a better understanding of the complex dynamics naturally occurring in wildlife populations. We aimed to approach the naturally occurring polyparasitism of gastrointestinal nematodes in a sympatric wild ruminant scenario present in south-east Spain. To this end, the gastrointestinal tract of 252 wild ruminants of four different species (red deer, Cervus elaphus; mouflon, Ovis aries musimon; Iberian ibex, Capra pyrenaica and fallow deer, Dama dama) were studied in Cazorla, Segura y Las Villas Natural Park (Andalusia, Spain). Of the analysed animals, 81.52% were positive for parasite infection and a total of 29 nematode species were identified. Out of these, 25 species were detected in at least two host species and 11 parasitized all ruminant species surveyed. The multi-host interaction between these nematodes and the four host species is discussed under the perspective of host family-based differences.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

These authors contributed equally to this study

References

Agosta, SJ and Klemens, JA (2008) Ecological fitting by phenotypically flexible genotypes: Implications for species associations, community assembly and evolution. Ecology Letters 11(11), 11231134.CrossRefGoogle ScholarPubMed
Agosta, SJ, Janz, N and Brooks, DR (2010) How specialists can be generalists: Resolving the “parasite paradox” and implications for emerging infectious disease. Zoologia (Curitiba) 27(2), 151162.CrossRefGoogle Scholar
Albon, SD, Stien, A, Irvine, RJ, Langvatn, R, Ropstad, E and Halvorsen, O (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London. Series B: Biological Sciences 269(1500), 16251632.CrossRefGoogle ScholarPubMed
Archie, EA and Ezenwa, VO (2011) Population genetic structure and history of a generalist parasite infecting multiple sympatric host species. International Journal for Parasitology 41(1), 8998.CrossRefGoogle ScholarPubMed
Arneberg, P (2001) An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24(3), 352358.CrossRefGoogle Scholar
Arneberg, P, Folstad, I and Karter, AJ (1996) Gastrointestinal nematodes depress food intake in naturally infected reindeer. Parasitology 112(2), 213219.CrossRefGoogle ScholarPubMed
Balicka-Ramisz, A, Laurans, L, Jurczyk, EW and Ramisz, A (2017) Gastrointestinal nematodes and the deworming of mouflon (Ovis aries musimon) from Goleniowska forest in west Pomerania province, Poland. Annals of Parasitology 63(1), 2732.Google ScholarPubMed
Bartczak, R and Okulewicz, A (2014) Epizootic situation of mouflon Ovis aries musimon in Lower Silesia on the basis of coproscopic examinations. Annals of Parasitology 60(4). ISO 690.Google ScholarPubMed
Boletín Oficial de la Junta de Andalucía—Boletín número 246 de 27/12/2017, 9 (2017). https://www.juntadeandalucia.es/boja/2017/246/BOJA17-246-00005-22369-01_00127264.pdfGoogle Scholar
Bordes, F, Morand, S, Kelt, DA and Van Vuren, DH (2009) Home range and parasite diversity in mammals. The American Naturalist 173(4), 467474.CrossRefGoogle ScholarPubMed
Brunner, FS and Eizaguirre, C (2016) Can environmental change affect host/parasite-mediated speciation? Zoology 119(4), 384394.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis. et al. Revisited. The Journal of Parasitology 83(4), 575583.CrossRefGoogle ScholarPubMed
Cassinello, J and Salvador Milla, A (2017) Muflón – Ovis orientalis Gmelin, 1774. 1st edn, 12 pp. Enciclopedia Virtual de los Vertebrados Españoles. Salvador, A., Barja, I. (Eds.). Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org/Google Scholar
Coltman, DW, Pilkington, JG, Smith, JA and Pemberton, jM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living island population. Evolution 53(4), 12591267.Google Scholar
Cornell, S (2005) Modelling nematode populations: 20 years of progress. Trends in Parasitology 21(11), 542545.CrossRefGoogle ScholarPubMed
Cox, FE (2001) Concomitant infections, parasites and immune responses. Parasitology 122(Suppl), S23S38.CrossRefGoogle ScholarPubMed
Craig, BH, Tempest, LJ, Pilkington, JG and Pemberton, JM (2008) Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135(4), 433441.CrossRefGoogle ScholarPubMed
De Leyva, E. (2002). Caza mayor y ganadería extensiva. 41, 1820.Google Scholar
Delogu, M, Ghetti, G, Gugiatti, A, Cotti, C, Piredda, I, Frasnelli, M and De Marco, MA (2013) Virological investigation of avian influenza virus on postglacial species of Phasianidae and Tetraonidae in the Italian Alps. ISRN Veterinary Science 2013, 601732.CrossRefGoogle ScholarPubMed
Dróżdż, J (1966) Studies on helminths and helminthiases in Cervidae. II. The helminth fauna in Cervidae in Poland. Acta Parasitologica Polonica 14(1/14), 113.Google Scholar
Durette-Desset, M-C (1989) Nomenclature proposée pour les espèces décrites dans la sous-famille des ostertagiinae Lopez-Neyra, 1947. Annales de Parasitologie Humaine et Comparée 64(5), 356373.CrossRefGoogle Scholar
Ezenwa, VO (2003) Habitat overlap and gastrointestinal parasitism in sympatric African bovids. Parasitology 126(4), 379388.CrossRefGoogle ScholarPubMed
Ezenwa, VO (2004) Parasite infection rates of impala (Aepyceros melampus) in fenced game reserves in relation to reserve characteristics. Biological Conservation 118(3), 397401.CrossRefGoogle Scholar
Fandos, P (1991) La cabra montés (Capra pyrenaica) en el Parque Natural de las Sierras de Cazorla, Segura y las Villas. 1st edn, 172 pp. s. Colección Técnica, Icona, Madrid.Google Scholar
Fanelli, A, Menardi, G, Chiodo, M, et al. (2020) Gastroenteric parasite of wild Galliformes in the Italian Alps: implication for conservation management. Parasitology 147(4), 471477.CrossRefGoogle ScholarPubMed
Gruijter, JMD, Ziem, J, Verweij, JJ, Polderman, AM and Gasser, RB (2004) Genetic substructuring within Oesophagostomum bifurcum (Nematoda) from human and non-human primates from Ghana based on random amplified polymorphic DNA analysis. The American Journal of Tropical Medicine and Hygiene 71(2), 227233.CrossRefGoogle ScholarPubMed
Gulland, FMD (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105(3), 493503.CrossRefGoogle ScholarPubMed
Gunn, A and Irvine, RJ (2003) Subclinical parasitism and ruminant foraging strategies: A review. Wildlife Society Bulletin 31(1), 117126.Google Scholar
Herlich, H (1965) The effects of the intestinal worms, Cooperia pectinata and Cooperia oncophora, on experimentally infected calves. American Journal of Veterinary Research 26(114), 10321036.Google ScholarPubMed
Herrera, AA (2008) Vertebrados del Plioceno Superior terminal en el suroeste de Europa: Fonelas p-1 y el proyecto Fonelas. 1st edn. Spain, 607 pp. s. Instituto Geológico y Minero de España.Google Scholar
Hoberg, EP and Brooks, DR (2008) A macroevolutionary mosaic: Episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35(9), 15331550.CrossRefGoogle Scholar
Hoberg, EP and Lichtenfels, JR (1994) Phylogenetic systematic analysis of the trichostrongylidae (Nematoda), with an initial assessment of coevolution and biogeography. The Journal of Parasitology 80(6), 976996.CrossRefGoogle Scholar
Hulme, PE, Roy, DB, Cunha, T, and Larsson, T-B (2009). A pan-European inventory of alien species: Rationale, implementation and implications for managing biological invasions. In Handbook of alien Species in Europe (pp. 114). Springer Netherlands.Google Scholar
Iacopelli, F, Fanelli, A, Tizzani, P, Berriatua, E, Prieto, P, Martínez-Carrasco, C, León, L, Rossi, L and Candela, MG (2020) Spatio-temporal patterns of sarcoptic mange in red deer and Iberian ibex in a multi-host natural park. Research in Veterinary Science 128, 224229.CrossRefGoogle Scholar
Ives, AR and Helmus, MR (2011) Generalized linear mixed models for phylogenetic analyses of community structure. Ecological Monographs 81(3), 511525.CrossRefGoogle Scholar
Jackson, F, Jackson, E and Williams, J (1988) Susceptibility of the pre-parturient ewe to infection with Trichostrongylus vitrinus and Ostertagia circumcincta. Research in Veterinary Science 45(2), 213218.CrossRefGoogle ScholarPubMed
Kelly, DW, Paterson, RA, Townsend, CR, Poulin, R and Tompkins, DM (2009) Parasite spillback: A neglected concept in invasion ecology? Ecology 90(8), 20472056.CrossRefGoogle ScholarPubMed
Lavín, S, Marco, I, Rossi, L, Meneguz, PG and Viñas, L (1997) Haemonchosis in Spanish ibex. Journal of Wildlife Diseases 33(3), 656659.CrossRefGoogle ScholarPubMed
Leivesley, JA, Bussière, LF, Pemberton, JM, Pilkington, JG, Wilson, K and Hayward, AD (2019) Survival costs of reproduction are mediated by parasite infection in wild Soay sheep. Ecology Letters 22(8), 12031213.Google ScholarPubMed
Margolis, L, Esch, GW, Holmes, JC, Kuris, AM and Schad, GA (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). The Journal of Parasitology 68(1), 131133.CrossRefGoogle Scholar
Martínez, T and Fandos, P (1989) Solapamiento entre la dieta de la cabra montés (capra pyrenaica) y la del muflón (Ovis musimon). Doñana, Acta Vertebrata 16(2), 315318.Google Scholar
Masseti, M and Mertzanidou, D (2008). Dama dama. The IUCN Red List of Threatened Species 2008: e.T42188A10656554. https://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T42188A10656554.en. Downloaded on 13 April 2021CrossRefGoogle Scholar
Miranda, M, Sicilia, M, Bartolomé, J, Molina-Alcaide, E, Gálvez-Bravo, L and Cassinello, J (2012) Contrasting feeding patterns of native red deer and two exotic ungulates in a Mediterranean ecosystem. Wildlife Research 39(2), 171182.CrossRefGoogle Scholar
Morand, S (2015) (Macro-) evolutionary ecology of parasite diversity: From determinants of parasite species richness to host diversification. International Journal for Parasitology: Parasites and Wildlife 4(1), 8087.Google ScholarPubMed
Morgan, ER, Milner-Gulland, EJ, Torgerson, PR and Medley, GF (2004) Ruminating on complexity: Macroparasites of wildlife and livestock. Trends in Ecology & Evolution 19(4), 181188.CrossRefGoogle ScholarPubMed
Obanda, V, Maingi, N, Muchemi, G, Ng'ang’a, CJ, Angelone, S and Archie, EA (2019) Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya. PLoS One 14(6), e0217929.CrossRefGoogle ScholarPubMed
Ocaido, M, Siefert, L and Baranga, J (2004) Helminth risks associated with mixed game and livestock interactions in and around Lake Mburo national park, Uganda. African Journal of Ecology 42(1), 4249.CrossRefGoogle Scholar
Ortiz, J, Ybáñez, MRRd, Garijo, MM, Goyena, M, Espeso, G, Abáigar, T and Cano, M (2001) Abomasal and small intestinal nematodes from captive gazelles in Spain. Journal of Helminthology 75(4), 363365.CrossRefGoogle ScholarPubMed
Ovaskainen, O and Soininen, J (2011) Making more out of sparse data: Hierarchical modeling of species communities. Ecology 92(2), 289295.CrossRefGoogle ScholarPubMed
Parker, GA, Chubb, JC, Ball, MA and Roberts, GN (2003) Evolution of complex life cycles in helminth parasites. Nature 425(6957), 480484.CrossRefGoogle ScholarPubMed
Parkins, JJ and Holmes, PH (1989) Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutrition Research Reviews 2(1), 227246.CrossRefGoogle ScholarPubMed
Pedersen, AB and Fenton, A (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22(3), 133139.CrossRefGoogle ScholarPubMed
Pisanu, B, Chapuis, JL, Et, C and Durette-Desset, MC (1996) Richesse spécifique en helminthes gastro-intestinaux du mouton (Ovis aries) et du mouflon (Ovis musimon) introduits dans l'archipel de kerguelen. Spécifie richness in gastrointestinal helminths front the domestic sheep (Ovis aries) and the Corsican mouflon (Ovis musimon) introduced onto the Kerguelen archipelago. Vie et Milieu 46, 305312.Google Scholar
Polley, L and Thompson, A (2015) Parasites and wildlife in a changing world. Trends in Parasitology 31(4), 123124.CrossRefGoogle Scholar
PORN (2017) Plan de ordenación de los recursos naturales del parque natural sierras de cazorla, segura y Las villas. Junta de Andalucía 246, 19352.Google Scholar
RStudio Team (2015) Studio: Integrated development for R. RStudio, PBC, Boston, MA. URL http://www.rstudio.com/.Google Scholar
Santín-Durán, M, Alunda, JM, Hoberg, EP and Fuente, Cdl (2004) Abomasal parasites in wild sympatric cervids, red deer, Cervus elaphus and fallow deer, Dama dama, from three localities across central and western Spain: Relationship to host density and park management. Journal of Parasitology 90(6), 13781386.CrossRefGoogle Scholar
Sinclair, R, Melville, L, Sargison, F, Kenyon, F, Nussey, D, Watt, K and Sargison, K (2016) Gastrointestinal nematode Species diversity in Soay sheep kept in a natural environment without active parasite control. Veterinary Parasitology 227, 17.CrossRefGoogle Scholar
Skrjabin, KI, Shikhobalova, NP, Schulz, RS, Popova, TI, Boev, SN and Delyamure, SL (1961) Key to parasitic Nematodes. Vol. III. Strongylata. 1st edn, 890 pp. Israel Program for Scientific Translations.Google Scholar
Smith, KF, Sax, DF and Lafferty, KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20(5), 13491357.CrossRefGoogle ScholarPubMed
Suarez, VH and Cabaret, J (1991) Similarities between species of the ostertagiinae (Nematoda: Trichostrongyloidea) in relation to host-specificity and climatic environment. Systematic Parasitology 20(3), 179185.CrossRefGoogle Scholar
Valcárcel, F and Romero, CG (1999) Prevalence and seasonal pattern of caprine trichostrongyles in a dry area of central Spain. Journal of Veterinary Medicine, Series B 46(10), 673681.CrossRefGoogle Scholar
Walker, JG and Morgan, ER (2014) Generalists at the interface: Nematode transmission between wild and domestic ungulates. International Journal for Parasitology: Parasites and Wildlife 3(3), 242250.Google Scholar
Wang, Y, Naumann, U, Wright, ST and Warton, DI (2012) Mvabund– an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3(3), 471474.CrossRefGoogle Scholar
Warwick, RM, Clarke, KR and Gee, JM (1990) The effect of disturbance by soldier crabs Mictyris platycheles H. Milne Edwards on meiobenthic community structure. Journal of Experimental Marine Biology and Ecology 135(1), 1933.CrossRefGoogle Scholar
Winter, J, Rehbein, S and Joachim, A (2018) Transmission of helminths between species of ruminants in Austria appears more likely to occur than generally assumed. Frontiers in Veterinary Science 5, 30.CrossRefGoogle ScholarPubMed
Yamaguti, S (1961) Systema helminthum. The Nematodes of vertebrates. 2 Vols. 1st edn, 679 pp. Interscience Publishers.Google Scholar
Yee, TW (2010) The VGAM package for categorical data analysis. Journal of Statistical Software 32(10), 134.CrossRefGoogle Scholar
Zaffaroni, E, Teresa Manfredi, M, Citterio, C, Sala, M, Piccolo, G and Lanfranchi, P (2000) Host specificity of abomasal nematodes in free ranging alpine ruminants. Veterinary Parasitology 90(3), 221230.CrossRefGoogle ScholarPubMed