Small mammal community composition impacts bank vole (Clethrionomys glareolus) population dynamics and associated seroprevalence of Puumala orthohantavirus

Abstract

Rodents are important reservoirs for zoonotic pathogens that cause diseases in humans. Biodiversity is hypothesized to be closely related to pathogen prevalence through multiple direct and indirect pathways. For example, the presence of non-host species can reduce contact rates of the main reservoir host and thus reduce the risk of transmission (“dilution effect”). In addition, an overlap in ecological niches between two species could lead to increased interspecific competition, potentially limiting host densities and reducing density-dependent pathogen transmission processes. In this study, we investigated the relative impact of population-level regulation of direct and indirect drivers of the prevalence of Puumala orthohantavirus (PUUV) in bank voles (Clethrionomys glareolus) during years with high abundance. We compiled data on small mammal community composition from four regions in Germany between 2010 and 2013. Structural equation modeling revealed a strong seasonality in PUUV control mechanisms in bank voles. The abundance of shrews tended to have a negative relationship with host abundance, and host abundance positively influenced PUUV seroprevalence, while at the same time increasing the abundance of competing non-hosts like the wood mouse (Apodemus sylvaticus) and the yellow-necked field mouse (Apodemus flavicollis) were associated with reduced PUUV seroprevalence in the host. These results indicate that for PUUV in bank voles, dilution is associated with increased interspecific competition. Anthropogenic pressures leading to the decline of Apodemus spp. in a specific habitat could lead to the amplification of mechanisms promoting PUUV transmission within the host populations.

Keywords

bank vole / biodiversity / Puumala orthohantavirus / small mammals

References

[1] Andreassen HP, Sundell J, Ecke F et al. (2021). Population cycles and outbreaks of small rodents: Ten essential questions we still need to solve. Oecologia 195, 601–622.

[2] Andrzejewski R, Olszewski J (1963). Social behaviour and interspecific relations in Apodemus flavicollis (Melchior,1834) and Clethrionomys glareolus (Schreber, 1780). Acta Theriologica 7, 155–168.

[3] Hille SM, Mortelliti A (2011). Microhabitat partitioning of Apodemus flavicollis and Myodes glareolus in the sub-montane Alps: A preliminary assessment. Hystrix, the Italian Journal of Mammalogy 21, 157–163.

[4] Binder F, Ryll R, Drewes S et al. (2020). Spatial and temporal evolutionary patterns in Puumala orthohantavirus (PUUV) S segment. Pathogens 9, 548.

[5] Boch S, Saiz H, Allan E et al. (2021). Direct and indirect effects of management intensity and environmental factors on the functional diversity of lichens in Central European forests. Microorganisms 9, 463.

[6] Boivin NL, Zeder MA, Fuller DQ et al. (2016). Ecological consequences of human niche construction: Examining long-term anthropogenic shaping of global species distributions. PNAS 113, 6388–6396.

[7] Bujalska G, Grüm L (2008). Interaction between populations of the bank vole and the yellow-necked mouse. Annales Zoologici Fennici 45, 248–254.

[8] Canova L (1993). Resource partitioning between the bank vole Clethrionomys glareolus and the wood mouse Apodemus sylvaticus in woodland habitats. Italian Journal of Zoology 60, 193–198.

[9] Carrick PJ, Forsythe KJ (2020). The species composition—ecosystem function relationship: A global meta-analysis using data from intact and recovering ecosystems. PLoS ONE 15, e0236550.

[10] Casula P, Luiselli L, Amori G (2019). Which population density affects home ranges of co-occurring rodents? Basic and Applied Ecology 34, 46–54.

[11] Drewes S, Ali HS, Saxenhofer M et al. (2017). Host-associated absence of human Puumala virus infections in Northern and Eastern Germany. Emerging Infectious Diseases 23, 83.

[12] Döhle HJ, Stubbe M, Lange U, Altner HJ (1984). Zur Dominanz-und Abundanzdynamik von Kleinnagern (Rodentia: Arvicolidae: Muridae) in Auwäldern der mittleren DDR. Säugetierkundliche Informationen 2, 115–136.

[13] Ecke F, Angeler DG, Magnusson M, Khalil H, Hörnfeldt B (2017). Dampening of population cycles in voles affects small mammal community structure, decreases diversity, and increases prevalence of a zoonotic disease. Ecology and Evolution 7, 5331–5342.

[14] Essbauer S, Schmidt J, Conraths FJ et al. (2006). A new Puumala hantavirus subtype in rodents associated with an outbreak of Nephropathia epidemica in South-East Germany in 2004. Epidemiology & Infection 134, 1333–1344.

[15] Fasola M, Canova L (2000). Asymmetrical competition between the bank vole and the wood mouse, a removal experiment. Acta Theriologica 45, 353–365.

[16] Fischer S, Mayer-Scholl A, Imholt C et al. (2018). Leptospira genomospecies and sequence type prevalence in small mammal populations in Germany. Vector-Borne and Zoonotic Diseases 18, 188–199.

[17] Hanski I (1991). The functional response of predators: Worries about scale. Trends in Ecology and Evolution 6, 141–142.

[18] Hansson L (1985). The food of bank voles, wood mice and yellow-necked mice. Symposia of the Zoological Society of London 55, 141–168.

[19] Haredasht SA, Taylor CJ, Maes P et al. (2013). Model-based prediction of Nephropathia epidemica outbreaks based on climatological and vegetation data and bank vole population dynamics. Zoonoses and Public Health 60, 461–477.

[20] Heyman P, Mele RV, Smajlovic L, Dobly A, Cochez C, Vandenvelde C (2009). Association between habitat and prevalence of hantavirus infections in bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus). Vector-Borne and Zoonotic Diseases 9, 141–146.

[21] Hotopp I, Walther B, Fuelling O et al. (2022). Habitat and season effects on small mammal bycatch in live trapping. Biology 11, 1806.

[22] Jacob J, Tkadlec E (2010). Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Banos, Philippines.

[23] Johnson CK, Hitchens PL, Pandit PS et al. (2020). Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proceedings of the Royal Society B 287, 20192736.

[24] Jones BA, Grace D, Kock R et al. (2013). Zoonosis emergence linked to agricultural intensification and environmental change. PNAS 110, 8399–83404.

[25] Jones KE, Patel NG, Levy MA et al. (2008). Global trends in emerging infectious diseases. Nature 451, 990–993.

[26] Kallio ER, Begon M, Henttonen H et al. (2010). Hantavirus infections in fluctuating host populations: The role of maternal antibodies. Proceedings of the Royal Society B: Biological Sciences 277, 3783–3791.

[27] Kallio ER, Poikonen A, Vaheri A et al. (2006). Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proceedings of the Royal Society B: Biological Sciences 273, 2771–2776.

[28] Keesing F, Holt RD, Ostfeld RS (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.

[29] Keesing F, Ostfeld RS (2021). Dilution effects in disease ecology. Ecology Letters 24, 2490–24505.

[30] Khalil H, Ecke F, Evander M, Magnusson M, Hörnfeldt B (2016). Declining ecosystem health and the dilution effect. Scientific Reports 6, 31314.

[31] Khalil H, Hörnfeldt B, Evander M, Magnusson M, Olsson G, Ecke F (2014). Dynamics and drivers of hantavirus prevalence in rodent populations. Vector-Borne and Zoonotic Diseases 14, 537–551.

[32] Leszek G, Bujalska G (2000). Bank voles and yellow-necked mice: What are interrelations between them? Polish Journal of Ecology 48, 141–145.

[33] Liesenjohann M, Liesenjohann T, Trebaticka L et al. (2011). From interference to predation: Type and effects of direct interspecific interactions of small mammals. Behavioral Ecology and Sociobiology 65, 2079–2089.

[34] Loreau M, De Mazancourt C (2013). Biodiversity and ecosystem stability: A synthesis of underlying mechanisms. Ecology Letters 16, 106–115.

[35] Magnusson M, Ecke F, Khalil H, Olsson G et al. (2015). Spatial and temporal variation of hantavirus bank vole infection in managed forest landscapes. Ecosphere 6, 1–18.

[36] Magnusson M, Fischhoff IR, Ecke F, Hörnfeldt B, Ostfeld RS (2020). Effect of spatial scale and latitude on diversity–disease relationships. Ecology 101, e02955.

[37] Marsh AC, Poulton S, Harris S (2001). The Yellow-necked Mouse Apodemus flavicollis in Britain: status and analysis of factors affecting distribution. Mammal Review 31, 203–227.

[38] Mcfarlane Ro, Sleigh A, Mcmichael T (2012). Synanthropy of wild mammals as a determinant of emerging infectious diseases in the Asian-Australasian region. Ecohealth 9, 24–35.

[39] Mertens M, Hofmann J, Petraityte-Burneikiene R et al. (2011). Seroprevalence study in forestry workers of a non-endemic region in eastern Germany reveals infections by Tula and Dobrava–Belgrade hantaviruses. Medical Microbiology and Immunology 200, 263–268.

[40] Mertens M, Wölfel R, Ullrich K et al. (2009). Seroepidemiological study in a Puumala virus outbreak area in South-East Germany. Medical Microbiology and Immunology 198, 83–91.

[41] Morand S (2020). Emerging diseases, livestock expansion and biodiversity loss are positively related at global scale. Biological Conservation 248, 108707.

[42] Nyholm NEI, Meurling P (1979). Reproduction of the bank vole, Clethrionomys glareolus, in northern and southern Sweden during several seasons and in different phases of the vole population cycle. Ecography 2, 12–20.

[43] Oksanen J, Blanchet FG, Kindt R et al. (2013). Package ‘vegan’. Community Ecology Package, Version 2, 1–295.

[44] Olsson GE, White N, Ahlm C et al. (2002). Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerging Infectious Diseases 8, 925.

[45] Palma RE, Polop JJ, Owen RD, Mills JN (2012). Ecology of rodent-associated hantaviruses in the Southern cone of South America: Argentina, Chile, Paraguay, and Uruguay. Journal of Wildlife Diseases 48, 267–281.

[46] Pievani T (2014). The sixth mass extinction: Anthropocene and the human impact on biodiversity. Rendiconti Lincei 25, 85–93.

[47] R Core Team (2023). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

[48] Randolph SE, Dobson ADM (2012). Pangloss revisited: A critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.

[49] Reil D, Imholt C, Eccard JA, Jacob J (2015). Beech fructification and bank vole population dynamics-combined analyses of promoters of human Puumala virus infections in Germany. PLoS ONE 10, e0134124.

[50] Reil D, Rosenfeld UM, Imholt C et al. (2017). Puumala hantavirus infections in bank vole populations: host and virus dynamics in Central Europe. BMC Ecology 17, 9.

[51] Rohr JR, Civitello DJ, Halliday FW et al. (2020). Towards common ground in the biodiversity–Disease debate. Nature Ecology & Evolution 4, 24–33.

[52] Rosseel Y (2012). lavaan: An R package for structural equation modeling. Journal of Statistical Software 48, 1–36.

[53] Schlegel M, Ali HS, Stieger N, Groschup MH, Wolf R, Ulrich RG (2012). Molecular identification of small mammal species using novel cytochrome B gene-derived degenerated primers. Biochemical Genetics 50, 440–447.

[54] Schmidt KA, Ostfeld RS (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.

[55] Stenseth NC, Viljugrein H, Jędrzejewski W, Mysterud A, Pucek Z (2002). Population dynamics of Clethrionomys glareolus and Apodemus flavicollis: Seasonal components of density dependence and density independence. Acta Theriologica 47, 39–67.

[56] Tersago K, Schreurs A, Linard C, Verhagen R, Van Dongen S, Leirs H (2008). Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence. Vector-Borne and Zoonotic Diseases 8, 235–244.

[57] Tersago K, Verhagen R, Servais A, Heyman P, Ducoffre G, Leirs H (2009). Hantavirus disease (nephropathia epidemica) in Belgium: Effects of tree seed production and climate. Epidemiology and Infection 137, 250–256.

[58] Tersago K, Verhagen R, Vapalahti O, Heyman P, Ducoffre G, Leirs H (2011). Hantavirus outbreak in Western Europe: Reservoir host infection dynamics related to human disease patterns. Epidemiology & Infection 139, 381–390.

[59] Thompson PL, Isbell F, Loreau M, O'connor MI, Gonzalez A (2018). The strength of the biodiversity–ecosystem function relationship depends on spatial scale. Proceedings of the Royal Society B 285, 20180038.

[60] Viviano A, Scarfò M, Mori E (2022). Temporal partitioning between forest-dwelling small rodents in a Mediterranean deciduous woodland. Animals 12, 279.

RIGHTS & PERMISSIONS

2023 2023 The Authors. Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.