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Macracanthorhynchus hirudinaceus in expanding wild boar (Sus scrofa) populations in Eastern Spain

  • Helminthology - Original Paper
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Abstract

Prevalence and temporal evolution of the infection by the acanthocephalan Macracanthorhynchus hirudinaceus is studied in the Valencian Community (Eastern Spain), a region only recently fully colonized by the expanding native Eurasian wild boar (Sus scrofa). For 8 years, a total of 1486 wild boars were sampled in order to look for the parasite. The mean prevalence was 20.7% (95% CI, 18.6–22.8; 307/1486). We observed an increasing trend through time, both in the number of wild boars and affected districts. The prevalence of M. hirudinaceus rose in parallel to the annual capture of wild boars, and its presence has been expanding towards the East. A hotspot of M. hirudinaceus is located to the west of the study area, in Muela de Cortes Game Reserve, where 89.6% of the wild boars were positive for the infection, constituting one of the world’s highest known prevalence areas.

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References

  • Abraham J, Giacomuzzi V, Angeli S (2015) Root damage to apple plants by cockchafer larvae induces a change in volatile signals below- and above-ground. Entomol Exp Appl 156:279–289. https://doi.org/10.1111/eea.12330

    Article  CAS  Google Scholar 

  • Acevedo P, Vicente J, Höfle U, Cassinelo J, Ruiz-Fons F (2006) Estimation of European wild boar relative abundance and aggregation: a novel method in epidemiological risk assessment. Epidemiol Infect 135:519–527

    Article  Google Scholar 

  • Anguix A, Díaz L (2008) gvSIG: A GIS desktop solution for an open SDI. J Geogr Reg Plann 1:041–048

    Google Scholar 

  • Barbosa JD, Silva JB, Reis ASB, Bomjardim HA, Driemeier D (2017) Identification of Macracanthorhynchus hirudinaceus, Stephanurus dentatus and Trichuris suis in native pigs of Marajó Island. J Vet Sci Med Diagn 6:4. https://doi.org/10.4172/2325-9590.1000237

    Article  Google Scholar 

  • BDB (2017) Banco de Datos de Biodiversidad de la Comunidad Valenciana http://www.bdb.gva.es/va/buscador

  • Boitani L, Mattei L (1992) Aging wild boar (Sus scrofa) by tooth eruption. In: Spitz F, Janeau G, Gonzalez G, Aulagnier S (eds) Ongulés/Ungulates. S.F.E.P.M.-I.R.G.M, París-Toulouse, pp 419–421

    Google Scholar 

  • Brianti E, Gaglio G, Ferlazzo M, Abbene S, Poglayen G, Gianetto S (2007) A review of parasites found in the Sicilian Black Pig. Proceedings of the 6th International Symposium on the Mediterranean Pig. October 11-13, 2007. Messina – Capo d’Orlando (ME), Italy

  • Burgui-Oltra JM, Navas-Almodóvar A, Nieto-Pérez MP (2017) Anexo I: Plan técnico de ordenación cinegética de la Reserva Valenciana de Caza de la Muela de Cortes. Temporadas 2017-18 a 2021-22. Direcció General de Medi Natural i d’Avaluació Ambiental. Generalitat Valenciana. Conselleria d’Agricultura, Medi Ambient, Canvi Climàtic i Desenvolupament rural. 132 pp., pages 52–60

  • de Estrada MBF (1997) Presentación del primer caso humano de parasitismo por Macracanthorhynchus hirudinaceus en el Perú y breve revisión. Revista Peruana de Medicina Experimental y Salud Publica. ISSN 1726-4634 Rev Peru Med Exp Salud Pública 14:47–50

  • De-la-Muela L, Hernández-de-Luján S, Ferre I (2001) Helminths of wild boar in Spain. J Wildl Dis 37:840–843

    Article  CAS  Google Scholar 

  • DOGV (2004) Ley 13/2004, de 27 de diciembre, de Caza de la Comunidad Valenciana. Diari Oficial de la Generalitat Valenciana. Núm. 4913 de 29.12.2004

  • DOGV (2012) ORDEN 3/2012, de 19 de enero, de la Conselleria de Infraestructuras, Territorio y Medio Ambiente, por la que se regula la caza y control del jabalí en la Comunitat Valenciana. Diari Oficial de la Generalitat Valenciana Núm. 6699 de 25.01.2012

  • Esteve C, Nieto MP (2017) Estadísticas cinegéticas de la Comunitat Valenciana. Memoria anual 2017. Informe interno del Servicio de Caza y Pesca. Generalitat Valenciana

  • Fernández-de-Mera IG, Gortazar C, Vicente J, Höfle U, Fierro Y (2003) Wild boar helminths: risk in animal translocations. Vet Parasitol 115:335–341

    Article  Google Scholar 

  • Foata J, Culioli JL, Marchand B (2005) Helminth fauna of wild boar in Corsica. Acta Parasitol 50:168–170

    Google Scholar 

  • Gassó D, Serrano E, Castillo-Contreras R, Fernández Aguilar X, Colom Cadena A, Velarde R, Mentaberre G, López-Olvera JR, Risco D, Gonçalves P, Lavín S, Fernandez-Llário P, Segalés J, Ferrer D (2016) Coprological tests underestimate Macracanthorhynchus hirudinaceus burden in wild boar. Parasitol Res 115:2103–2105

    Article  Google Scholar 

  • Geisser H, Reyer HU (2004) Efficacy of hunting, feeding, and fencing to reduce crop damage by wild boars. J Wildl Manag 68:939–946. https://doi.org/10.2193/0022-541X(2004)068[0939:EOHFAF]2.0.CO;2

    Article  Google Scholar 

  • Giménez-Anaya A, Herrero J, Rosell C, Couto S, García-Serrano A (2008) Food habits of wild boars (Sus scrofa) in a Mediterranean coastal wetland. Wetlands 28:197–203. https://doi.org/10.1672/07-18.1

    Article  Google Scholar 

  • Hamula CL, Fang DC, Couturier MR (2014) Photo quiz: an unwelcome passenger in a 17-month-old male. J Clin Microbiol 52:2289. https://doi.org/10.1128/jcm.00280-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Herrero J, García-Serrano A, Couto S, Ortuño VM, García-González R (2006) Diet of wild boar Sus scrofa L. and crop damage in an intensive agroecosystem. Eur J Wildl Res 52:245–250. https://doi.org/10.1007/s10344-006-0045-3

    Article  Google Scholar 

  • Humbert JF, Henry C (1989) Studies on the prevalence and the transmission of lung and stomach nematodes of the wild boar (Sus scrofa) in France. J Wildl Dis 25:335–341

    Article  CAS  Google Scholar 

  • ICV. Institut Cartogràfic Valencià (2018) Unidades administrativas: Delimitación comarcal en la Comunitat Valenciana. http://descargas.icv.gva.es/server_api/gdb/descarga/index.html?capas = % 22ign_limits.gdb/ign_limcomarcal_pol%22&formato = Shapefile%20-%20SHP%20-%20.shp&g eocat = DATO_DIRECTA_SHP. Accessed on 27 Sept 2019

  • ICV. Institut Cartogràfic Valencià (2019) Corine Land Cover año 2018. http://www.icv.gva.es/auto/aplicaciones/icv_geocat/#/search?uuid = spa_icv_suelo_corine2018_cv&lang = spa. Accessed on 30 Oct 2019

  • IGME. Instituto Geológico y Minero de España (2014) Geológico Comunidad Valenciana 400. http://mapas.igme.es/gis/rest/services/Cartografia_Geologica/IGME_GeologicoCValenciana_400/MapServer. Accesed on 12 Oct 2019

  • Jackson TA, Klein MG (2006) Scarabs as pests: a continuing problem. Coleopt Bull 60(Monogr 5):102–119. https://doi.org/10.1649/0010-065X(2006)60[102:SAPACP]2.0.CO;2

    Article  Google Scholar 

  • Johnson SN, Nielsen U (2012) Foraging in the dark—chemically mediated host location by root-feeding insects. J Chem Ecol 38:604–614

    Article  CAS  Google Scholar 

  • Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263. https://doi.org/10.1127/0941-2948/2006/0130

    Article  Google Scholar 

  • Leng YJ, Huang WD, Liang PN (1983) Human infection with Macracanthorhynchus hirudinaceus Travassos, 1916 in Guangdong Province, with notes on its prevalence in China. Ann Trop Med Parasitol 77:107–109. https://doi.org/10.1080/00034983.1983.11811681

    Article  CAS  PubMed  Google Scholar 

  • Mansouri M, Sarkari B, Mowlavi GR (2016) Helminth parasites of wild boars, Sus scrofa, in Bushehr Province, Southwestern Iran. Iran J Parasitol 11:377–382

    PubMed  PubMed Central  Google Scholar 

  • Massei G, Kindberg J, Licoppe A, Gačić D, Šprem N, Kamler J, Baubet E, Hohmann U, Monaco A, Ozolin J, Cellina S, Podgórski T, Fonseca C, Markov N, Pokorny B, Rosell C, Náhlik A (2015) Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag Sci 71:492–500

    Article  CAS  Google Scholar 

  • Mowlavi GR, Massoud J, Mobedi I, Solaymani-Mohammadi S, Gharagozlou MJ, Mas-Coma S (2006) Very highly prevalent Macracanthorhynchus hirudinaceus infection of wild boar Sus scrofa in Khuzestan province, south-western Iran. Helminthologia 43:86–91. https://doi.org/10.2478/s11687-006-0017-x

    Article  Google Scholar 

  • Nagy G, Ács K, Varga G, Sugár L, Csivincsik Á (2015) Macracanthorhynchus hirudinaceus (Pallas, 1781) larvae in cockchafer (Melolontha spp.) grubs in different habitat conditions. Eur J Wildl Res 61:487–489

    Article  Google Scholar 

  • Nansen P, Roepstor A (1999) Parasitic helminths of the pig: factors influencing transmission and infection levels. Int J Parasitol 29:877–891

    Article  CAS  Google Scholar 

  • Navarro-González N, Fernández-Llario P, Pérez-Martín JE, Mentaberre G, López-Martín JM, Lavín S, Serrano E (2013) Supplemental feeding drives endoparasite infection in wild boar in Western Spain. Vet Parasitol 196:114–123

    Article  Google Scholar 

  • Neafie RC, Marty AM (2000) Acanthocephaliasis. In: Meyers WM, Neafie RC, Marty AM and Wear DJ (Eds): Pathology of infectious diseases, vol. 1 helminthiases. Armed Forces Institute of Pathology and American Registry of Pathology, Washington D.C.: 519–529

  • Reiczigel J, Marozzi M, Fabian I, Rozsa L (2019) Biostatistics for parasitologists – a primer to quantitative parasitology. Trends Parasitol 35:277–281

    Article  Google Scholar 

  • Reinecke A, Mueller F, Hilker M (2008) Attractiveness of CO2 released by root respiration fades on the background of root exudates. Basic Appl Ecol 9:568–576

    Article  CAS  Google Scholar 

  • Ruiz-Fons F, Segalés J, Gortázar C (2008) A review of viral diseases of the European wild boar: effects of the population dynamics and reservoir role. Vet J 176:158–169

    Article  Google Scholar 

  • Sarkari B, Mansouri M, Najjari M, Derakhshanfar A, Mowlavi GR (2016) Macracanthorhynchus hirudinaceus: the most common helminthic infection of wild boars in southwestern Iran. J Parasit Dis 40:1563–1566. https://doi.org/10.1007/s12639-015-0728-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt GD (1971) Acanthocephalan infections of man, with two new records. J Parasitol 57:582–584. https://doi.org/10.2307/3277920

    Article  CAS  PubMed  Google Scholar 

  • Senlik B, Cirak VY, Girisgin O, Akyol CV (2011) Helminth infections of wild boars (Sus scrofa) in the Bursa province of Turkey. J Helminthol 85:404–408

    Article  CAS  Google Scholar 

  • Solaymani-Mohammadi S, Mobedi I, Rezaian M, Massoud J, Mohebali M, Hooshyar H, Ashrafi K, Rokni MB (2003) Helminth parasites of the wild boar, Sus scrofa, in Luristan province, western Iran and their public health significance. J Helminthol 77:263–267. https://doi.org/10.1079/joh2003168

    Article  CAS  PubMed  Google Scholar 

  • Stumpf IVK (1986) Hospedeiros intermediários de Macracanthorynchus hirudinaceus (Pallas, 1781) (Acanthocephala) em Mandirituba, Paraná, Brasil. Acta Biol Parana 15:87–124

    Google Scholar 

  • Svestka M (2007) Ecological conditions influencing the localization of egg-laying by females of the cockchafer (Melolontha hippocastani F.). J For Sci 53:16–24

    Article  Google Scholar 

  • Svetska M (2006) Distribution of tribes of cockchafers of the genus Melolontha in forests of the Czech Republic and the dependence of their swarming on temperature. J For Sci 52:520–530

    Google Scholar 

  • Taylor MA, Coop RL, Wall RL (2015) Veterinary parasitology, 4th Edition. ISBN: 978-0-470-67162-7. Wiley Blackwell. Chichester

  • Zhong HL, Feng LB, Wang CX (1983) Human infection with Macracanthorhynchus hirudinaceus causing serious complications in China. Chin Med J 96:661–668

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors wish to express their gratitude to Iris García-Bacete and Ismael Pérez-López for their involvement and diligence in field tasks and to Danielle Greenspan and Paul John Schnyder for English language editing and revision. Finally, we would like to thank the two anonymous reviewers for their suggestions and comments.

Funding

This research was partially supported by Banco Santander grant FUSPBS-PPC13/2016 and by Conselleria d’Agricultura, Medi Ambient, Canvi Climàtic i Desenvolupament Rural of Generalitat Valenciana, through the minor contracts 2013/21/187 and 2014/21/112.

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Authors

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Conceptualization: Victor Lizana, Miguel Angel Sanchez-Isarria

Formal analysis and investigation: Victor Lizana, Raquel Prats, Jesus Cardells

Writing – original draft preparation: Victor Lizana, Maria Jose Carrion, Jesus Cardells

Writing – review and editing: Christian Gortazar

Funding acquisition: Miguel Angel Sanchez-Isarria

Supervision: Christian Gortazar

Corresponding author

Correspondence to Victor Lizana.

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The authors declare that they have no conflict of interest.

Ethics approval

All animal sampling took place post-mortem. The wildlife samples were obtained from hunter-harvested individuals that were hunted independently for our research. According to EU and National legislation (2010/63/UE Directive and Spanish Royal Decree 53/2013) and to the University of Castilla—La Mancha guidelines, no permission or consent is required to conduct the research reported herein.

Bioethics Commission of the CEU Cardenal Herrera University, through report 20/013, decided that no special authorization was necessary, given that the samples were taken post-mortem.

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Section Editor: Hiroshi Sato

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Lizana, V., Gortazar, C., Prats, R. et al. Macracanthorhynchus hirudinaceus in expanding wild boar (Sus scrofa) populations in Eastern Spain. Parasitol Res 120, 919–927 (2021). https://doi.org/10.1007/s00436-020-06975-y

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