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Zoonotic pathogens in fluctuating common vole (Microtus arvalis) populations: occurrence and dynamics

Published online by Cambridge University Press:  24 September 2018

Ruth Rodríguez-Pastor Open the ORCID record for Ruth Rodríguez-Pastor [Opens in a new window] ,
Raquel Escudero ,
Xavier Lambin Open the ORCID record for Xavier Lambin [Opens in a new window] ,
Mª Dolors Vidal ,
Horacio Gil ,
Isabel Jado ,
Manuela Rodríguez-Vargas ,
Juan José Luque-Larena  and
François Mougeot Open the ORCID record for François Mougeot [Opens in a new window]
Ruth Rodríguez-Pastor*
Affiliation:
Dpto. Ciencias Agroforestales, ETSIIAA, Universidad de Valladolid, Avda. de Madrid 44, 34004, Palencia, Spain Instituto Universitario de Investigación en Gestión Forestal Sostenible, Palencia, Spain
Raquel Escudero
Affiliation:
Laboratorio de Referencia e Investigación en Patógenos Especiales. Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220, Majadahonda, Madrid, Spain
Xavier Lambin
Affiliation:
School of Biological Sciences, University of Aberdeen, Aberdeen, UK
Mª Dolors Vidal
Affiliation:
Área de Microbiología, Facultad de Medicina, Universidad de Castilla-La Mancha, 13071, Ciudad Real, Spain
Horacio Gil
Affiliation:
Laboratorio de Referencia e Investigación en Patógenos Especiales. Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220, Majadahonda, Madrid, Spain
Isabel Jado
Affiliation:
Laboratorio de Referencia e Investigación en Patógenos Especiales. Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220, Majadahonda, Madrid, Spain
Manuela Rodríguez-Vargas
Affiliation:
Laboratorio de Referencia e Investigación en Patógenos Especiales. Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220, Majadahonda, Madrid, Spain
Juan José Luque-Larena
Affiliation:
Dpto. Ciencias Agroforestales, ETSIIAA, Universidad de Valladolid, Avda. de Madrid 44, 34004, Palencia, Spain Instituto Universitario de Investigación en Gestión Forestal Sostenible, Palencia, Spain
François Mougeot
Affiliation:
Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071, Ciudad Real, Spain
*
Author for correspondence: Ruth Rodríguez-Pastor, E-mail: ruth.rodriguez@uva.es
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Abstract

Diseases and host dynamics are linked, but their associations may vary in strength, be time-lagged, and depend on environmental influences. Where a vector is involved in disease transmission, its dynamics are an additional influence, and we often lack a general understanding on how diseases, hosts and vectors interact. We report on the occurrence of six zoonotic arthropod-borne pathogens (Anaplasma, Bartonella, Borrelia, Coxiella, Francisella and Rickettsia) in common voles (Microtus arvalis) throughout a population fluctuation and how their prevalence varies according to host density, seasonality and vector prevalence. We detected Francisella tularensis and four species of Bartonella, but not Anaplasma, Borrelia, Coxiella or Rickettsia. Bartonella taylorii and B. grahamii prevalence increased and decreased with current host (vole and mice) density, respectively, and increased with flea prevalence. Bartonella doshiae prevalence decreased with mice density. These three Bartonella species were also more prevalent during winter. Bartonella rochalimae prevalence varied with current and previous vole density (delayed-density dependence), but not with season. Coinfection with F. tularensis and Bartonella occurred as expected from the respective prevalence of each disease in voles. Our results highlight that simultaneously considering pathogen, vector and host dynamics provide a better understanding of the epidemiological dynamics of zoonoses in farmland rodents.

Keywords

BartonellafleasFrancisella tularensisrodent- and arthropod-borne pathogensMicrotus arvalismixed infectionspopulation outbreakszoonotic diseases dynamics
Type
Research Article
Information
Parasitology , Volume 146 , Issue 3 , March 2019 , pp. 389 - 398
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Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

*

These authors contributed equally.

†

Equal supervision.

References

Anda, P, Escudero, R, Rodriguez-Moreno, I, Jado, I and Jimenez-Alonso, MI (2012) Method and kit for the detection of bacterial species by means of DNA. EP1895015B1.Google Scholar
Bandouchova, H, Sedlackova, J, Pohanka, M, Novotny, L, Hubalek, M, Treml, F, Vitula, F and Pikula, J (2009) Tularemia induces different biochemical responses in BALB/c mice and common voles. BMC Infectious Diseases 9, 101.Google Scholar
Barandika, JF, Hurtado, A, García-Esteban, C, Gil, H, Escudero, R, Barral, M, Jado, I, Juste, RA, Anda, P and García-Pérez, AL (2007) Tick-borne zoonotic bacteria in wild and domestic small mammals in Northern Spain. Applied and Environmental Microbiology 73, 6166–6171.Google Scholar
Bibikova, VA (1977) Contemporary views on the interrelationships between fleas and the pathogens of human and animal diseases. Annual Review of Entomology 22, 23–32.Google Scholar
Birtles, RJ (2005) Bartonellae as elegant hemotropic parasites. In Oteo, JA, Hechemy, KE, Raoult, DA, Silverman, DJ and Blanco, JR (eds), Rickettsioses: From Genome to Proteome, Pathobiology, and Rickettsiae as an International Threat, vol. 1063. Annals of the New York Academy of Science, pp. 270–279.Google Scholar
Bonita, R, Beaglehole, R and Kjellström, T (2006) Basic Epidemiology, 2nd Edn. Geneva, Switzerland: World Health Organization. http://apps.who.int/iris/bitstream/handle/10665/43541/9241547073_eng.pdf?sequence=1.Google Scholar
Buffet, JP, Marsot, M, Vaumourin, E, Gasqui, P, Masséglia, S, Marcheteau, E, Huet, D, Chapuis, J-L, Pisanu, B, Ferquel, E, Halos, L, Vourc'h, G and Vayssier-Taussat, M (2012) Co-infection of Borrelia afzelii and Bartonella spp. in bank voles from a suburban forest. Comparative Immunology, Microbiology and Infectious Diseases 35, 583–589.Google Scholar
Dicker, R, Coronado, F, Koo, D and Parrish, RG (2011) Principles of Epidemiology in Public Health Practice, 3rd Edn. Centers for Disease Control and Prevention. https://www.cdc.gov/ophss/csels/dsepd/ss1978/index.html.Google Scholar
Cevidanes, A, Altet, L, Chirife, AD, Proboste, T and Millán, J (2017) Drivers of Bartonella infection in micromammals and their fleas in a Mediterranean peri-urban area. Veterinary Microbiology 203, 181–188.Google Scholar
Chang, CC, Chomel, BB, Kasten, RW, Romano, V and Tietze, N (2001) Molecular evidence of Bartonella spp. in questing adult Ixodes pacificus ticks in California. Journal of Clinical Microbiology 39, 1221–1226.Google Scholar
Cox, FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122(Suppl.), S23–S38.Google Scholar
Escudero, R, Toledo, A, Gil, H, Kovacsova, K, Rodriguez-Vargas, M, Jado, I, Garcia-Amil, C, Lobo, B, Bhide, M and Anda, P (2008) Molecular method for discrimination between Francisella tularensis and Francisella-like endosymbionts. Journal of Clinical Microbiology 46, 3139–3143.Google Scholar
Fischer, S, Spierling, NG, Heuser, E, Kling, C, Schmidt, S, Rosenfeld, UM, Reil, D, Imholt, C, Jacob, J, Ulrich, RG and Essbauer, S (2018) High prevalence of Rickettsia helvetica in wild small mammal populations in Germany. Ticks and Tick-borne Diseases 9, 500–505.Google Scholar
Garcia-Esteban, C, Gil, H, Rodriguez-Vargas, M, Gerrikagoitia, X, Barandika, J, Escudero, R, Jado, I, Garcia-Amil, C, Barral, M, Garcia-Perez, AL, Bhide, M and Anda, P (2008) Molecular method for Bartonella species identification in clinical and environmental samples. Journal of Clinical Microbiology 46, 776–779.Google Scholar
Gil, H, Barral, M, Escudero, R, Garcia-Perez, AL and Anda, P (2005) Identification of a new Borrelia species among small mammals in areas of Northern Spain where Lyme disease is endemic. Applied and Environmental Microbiology 71, 1336–1345.Google Scholar
Gil, H, García-Esteban, C, Barandika, JF, Peig, J, Toledo, Á, Escudero, R, Jado, I, Rodríguez-Vargas, M, García-Amil, C, Lobo, B, Roales, P, Rodríguez-Moreno, I, Olmeda, AS, García-Pérez, AL and Anda, P (2010) Variability of Bartonella genotypes among small mammals in Spain. Applied and Environmental Microbiology 76, 8062–8070.Google Scholar
Gómez López, MS, Martín Mateo, MP and Martínez, MD (2004) Malófagos, anopluros y sifonápteros. In Barrientos, JA (ed.), Curso Práctico de Entomología. Asociación Española de Entomología, CIBIO: Centro Iberoamericano de Biodiversidad (Alicante), Universitat Autònoma de Barcelona, pp. 599–614.Google Scholar
Gratz, NG (1994) Rodents and human disease: a global appreciation. In Buckle, AP and Smith, RH (eds), Rodent Pests and Their Control. Wallingford (UK): CAB International, pp. 101–169.Google Scholar
Gutiérrez, R, Krasnov, B, Morick, D, Gottlieb, Y, Khokhlova, IS and Harrus, S (2015) Bartonella infection in rodents and their flea ectoparasites: an overview. Vector-Borne and Zoonotic Diseases 15, 27–39.Google Scholar
Han, BA, Schmidt, JP, Bowden, se and Drake, JM (2015) Rodent reservoirs of future zoonotic diseases. PNAS 112, 7039–7044.Google Scholar
Harms, A and Dehio, C (2012) Intruders below the radar: molecular pathogenesis of Bartonella spp. Clinical Microbiology Reviews 25, 42–78.Google Scholar
Hopla, CE (1974) The ecology of tularemia. Advances in Veterinary Science and Comparative Medicine 18, 25–53.Google Scholar
Jacob, J and Tkadlec, E (2010) Rodent outbreaks in Europe: dynamics and damage. In Singleton, GR, Belmain, S, Brown, PR and Hardy, B (eds), Rodent Outbreaks – Ecology and Impacts. Los Baños, Philippines: International Rice Research Institute, pp. 207–223.Google Scholar
Jareño, D, Viñuela, J, Luque-Larena, JJ, Arroyo, L, Arroyo, B and Mougeot, F (2015) Factors associated with the colonization of agricultural areas by common voles Microtus arvalis in NW Spain. Biological Invasions 17, 2315–2327.Google Scholar
Jolles, AE, Ezenwa, VO, Etienne, RS, Turner, WC and Olff, H (2008) Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89, 2239–2250.Google Scholar
Kallio, ER, Begon, M, Birtles, RJ, Bown, KJ, Koskela, E, Mappes, T and Watts, PC (2014) First report of Anaplasma phagocytophilum and Babesia microti in rodents in Finland. Vector-Borne and Zoonotic Diseases 14, 389–393.Google Scholar
Koskela, KA, Kalin-Mänttäri, L, Hemmilä, H, Smura, T, Kinnunen, PM, Niemimaa, J, Henttonen, H and Nikkari, S (2017) Metagenomic evaluation of bacteria from voles. Vector-Borne and Zoonotic Diseases 17, 123–133.Google Scholar
Kosoy, MY, Regnery, RL, Kosaya, OI, Jones, DC, Marston, EL and Childs, JE (1998) Isolation of Bartonella spp. from embryos and neonates of naturally infected rodents. Journal of Wildlife Diseases 34, 305–309.Google Scholar
Lambin, X, Bretagnolle, V and Yoccoz, NG (2006) Vole population cycles in northern and Southern Europe: is there a need for different explanations for single pattern? Journal of Animal Ecology 75, 340–349.Google Scholar
Luque-Larena, JJ, Mougeot, F, Viñuela, J, Jareño, D, Arroyo, L, Lambin, X and Arroyo, B (2013) Recent large-scale range expansion and outbreaks of the common vole (Microtus arvalis) in NW Spain. Basic and Applied Ecology 14, 432–441.Google Scholar
Luque-Larena, JJ, Mougeot, F, Roig, DV, Lambin, X, Rodríguez-Pastor, R, Rodríguez-Valín, E, Anda, P and Escudero, R (2015) Tularemia outbreaks and common vole (Microtus arvalis) irruptive population dynamics in Northwestern Spain, 1997–2014. Vector-Borne and Zoonotic Diseases 15, 568–570.Google Scholar
Luque-Larena, JJ, Mougeot, F, Arroyo, B, Vidal, D, Rodríguez-Pastor, R, Escudero, R, Anda, P and Lambin, X (2017) Irruptive mammal host populations shape tularemia epidemiology. PLoS Pathogens 13, e1006622.Google Scholar
Márquez, FJ, Rodríguez-Liébana, JJ, Pachón-Ibáñez, ME, Docobo-Pérez, F, Hidalgo-Fontiveros, A, Bernabeu-Wittel, M, Muniain, MA and Pachón, J (2008) Molecular screening of Bartonella species in rodents from South Western Spain. Vector-Borne and Zoonotic Diseases 8, 695–700.Google Scholar
Meerburg, BG, Singleton, GR and Kijlstra, A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35, 221–270.Google Scholar
Morner, T, Obendorf, DL, Artois, M and Woodford, MH (2002) Surveillance and monitoring of wildlife diseases. Revue Scientifique et Technique de l'OIE 21, 67–76.Google Scholar
Oporto, B, Gil, H, Barral, M, Hurtado, A, Juste, RA and Garcia-Perez, AL (2003) A survey on Anaplasma phagocytophila in wild small mammals and roe deer (Capreolus capreolus) in Northern Spain. Annals of the New York Academy of Science 990, 98–102.Google Scholar
Paziewska, A, Harris, PD, Zwolińska, L, Bajer, A and Siński, E (2012) Differences in the ecology of Bartonella infections of Apodemus flavicollis and Myodes glareolus in a boreal forest. Parasitology 139, 881–893.Google Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Razzauti, M, Galan, M, Bernard, M, Maman, S, Klopp, C, Charbonnel, N, Vayssier-Taussat, M, Eloit, M and Cosson, J-F (2015) A comparison between transcriptome sequencing and 16S metagenomics for detection of bacterial pathogens in wildlife. PLoS Neglected Tropical Diseases 9, e0003929.Google Scholar
Rodríguez-Pastor, R, Luque-Larena, JJ, Lambin, X and Mougeot, F (2016) ‘Living on the edge’: the role of field margins for common vole (Microtus arvalis) populations in recently colonised Mediterranean farmland. Agriculture, Ecosystems and Environment 231, 206–217.Google Scholar
Rodríguez-Pastor, R, Escudero, R, Vidal, D, Mougeot, F, Arroyo, B, Lambin, X, Vila-Coro, AM, Rodríguez-Moreno, I, Anda, P and Luque-Larena, JJ (2017) Density-dependent prevalence of Francisella tularensis in fluctuating vole populations, Northwestern Spain. Emerging Infectious Diseases 23, 1377–1379.Google Scholar
Rossow, H, Forbes, KM, Tarkka, E, Kinnunen, PM, Hemmilä, H, Huitu, O, Nikkari, S, Henttonen, H, Kipar, A and Vapalahti, O (2014) Experimental infection of voles with Francisella tularensis indicates their amplification role in tularemia outbreaks. PLoS ONE 9, e108864.Google Scholar
Rossow, H, Ollgren, J, Hytonen, J, Rissanen, H, Huitu, O, Henttonen, H, Kuusi, M and Vapalahti, O (2015) Incidence and seroprevalence of tularaemia in Finland, 1995 to 2013: regional epidemics with cyclic pattern. Euro Surveillance 20, 21209.Google Scholar
Silaghi, C, Woll, D, Hamel, D, Pfister, K, Mahling, M and Pfeffer, M (2012) Babesia spp. and Anaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents – analyzing the host-pathogen-vector interface in a metropolitan area. Parasites & Vectors 5, 191.Google Scholar
Silaghi, C, Pfeffer, M, Kiefer, D, Kiefer, M and Obiegala, A (2016) Bartonella, rodents, fleas and ticks: a molecular field study on host-vector-pathogen associations in Saxony, Eastern Germany. Microbial Ecology 72, 965–974.Google Scholar
Smith, A, Telfer, S, Burthe, S, Bennett, M and Begon, M (2005) Trypanosomes, fleas and field voles: ecological dynamics of a host-vector-parasite interaction. Parasitology 131, 355–365.Google Scholar
Telfer, S, Begon, M, Bennett, M, Bown, KJ, Burthe, S, Lambin, X, Telford, G and Birtles, R (2007 a) Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology 134, 413–425.Google Scholar
Telfer, S, Clough, HE, Birtles, RJ, Bennett, M, Carslake, D, Helyar, S and Begon, M (2007 b) Ecological differences and coexistence in a guild of microparasites: Bartonella in wild rodents. Ecology 88, 1841–1849.Google Scholar
Telfer, S, Lambin, X, Birtles, R, Beldomenico, P, Burthe, S, Paterson, S and Begon, M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243–246.Google Scholar
Tkadlec, E and Stenseth, NC (2001) A new geographical gradient in vole population dynamics. Proceedings of the Royal Society B: Biological Sciences 268, 1547–1552.Google Scholar
Versage, JL, Severin, DDM, Chu, MC and Petersen, JM (2003) Development of a multitarget real-time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. Journal of Clinical Microbiology 41, 5492–5499.Google Scholar
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