Abstract
Land-use change can raise the risk of human exposure to zoonotic diseases by increasing abundance of reservoir hosts. In this study, we conducted a meta-analysis on the associations between land-use change and the abundance of rodent species in relation to their reservoir status for rodent-borne diseases. Using the PREDICT database, we analyzed 58 case studies comprising 54 species from eight countries. In general, rodent reservoirs were significantly more abundant in modified habitats (anthropogenically altered sites), whereas non-reservoir species were more abundant in non-modified habitats. To our knowledge, this is the first meta-analysis that evaluates the response of rodents to land-use change with a focus on the potential implications for epidemiological risks. Our findings give further evidence that land-use change generally impacts biodiversity in ways that might imply higher risk of zoonotic pathogen transmission.
This is a preview of subscription content, log in via an institution to check access.
References
Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M et al (2017) Global hotspots and correlates of emerging zoonotic diseases. Nat Commun 8:1124. https://doi.org/10.1038/s41467-017-00923-8
Bai Y, Kosoy MY, Calisher CH, Cully JF, Collinge SK (2009) Effects of rodent community diversity and composition on prevalence of an endemic bacterial pathogen-Bartonella. Biodiversity 10:3–11
Begon M, Bennett M, Bowers RG, French NP, Hazel SM, Turner J (2002) A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiol Infect 129:147–153. https://doi.org/10.1017/S0950268802007148
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical. Br Med J 316:469–469
Foley JE, Nieto NC, Foley P (2009) Emergence of tick-borne granulocytic anaplasmosis associated with habitat type and forest change in northern California. Am J Trop Med Hyg 81:1132–1140. https://doi.org/10.4269/ajtmh.2009.09-0372
Gage KL, Kosoy MY (2005) Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50:505–528. https://doi.org/10.1146/annurev.ento.50.071803.130337
García KP, Ortiz JC, Aguayo M, D’Elia G (2013) Assessing rodent community responses in disturbed environments of the Chilean Patagonia. Mammalia 77:195–204. https://doi.org/10.1515/mammalia-2011-0134
Garmendia A, Arroyo-Rodriguez V, Estrada A, Naranjo EJ, Stoner KE (2013) Landscape and patch attributes impacting medium- and large- sized terrestrial mammals in a fragmented rain forest. J Trop Ecol 29:331–344. https://doi.org/10.1017/S0266467413000370
Gheler-Costa C, Vettorazzi CA, Pardini R, Verdade LM (2012) The distribution and abundance of small mammals in agroecosystems of southeastern Brazil. Mammalia 76:185–191. https://doi.org/10.1515/mammalia-2011-0109
Gottdenker NL, Streicker DG, Faust CL, Carrol CR (2014) Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth 11:619–632. https://doi.org/10.1007/s10393-014-0941-z
Granjon L, Duplantier J (2011) Guinean biodiversity at the edge: rodents in forest patches of southern Mali. Mamm Biol 76:583–591
Guo F, Bonebrake TC, Gibson L (2018) Land-use change alters host and vector communities and may elevate disease risk. EcoHealth 1–12. https://doi.org/10.1007/s10393-018-1336-3
Han BA, Schmidt SP, Bowden SE, Drake JM (2015) Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci U S A 112:22. https://doi.org/10.1073/pnas.1501598112
Han BA, Kramer AM, Drake JM (2016) Global patterns of zoonotic disease in mammals. Trends Parasitol 32:565–577. https://doi.org/10.1016/j.pt.2016.04.007
Hudson LN, Newbold T, Contu S, Hill SL, Lysenko I, De Palma A et al (2017) The database of the PREDICTS (projecting responses of ecological diversity in changing terrestrial systems) project. Ecol Evol 7:145–188. https://doi.org/10.1002/ece3.2579
Jarquín-Díaz VH, Balard A, Jost J, Kraft J, Dikmen MN, Kvičerová J, Heitlinger E (2019) Detection and quantification of house mouse Eimeria at the species level – challenges and solutions for the assessment of coccidia in wildlife. Int J Parasitol Parasites Wildl 10:29–40. https://doi.org/10.1016/j.ijppaw.2019.07.004
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993. https://doi.org/10.1038/nature06536
Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498. https://doi.org/10.1111/j.1461-0248.2006.00885.x
Keinath DA, Doak DF, Hodges KE, Prugh LR, Fagan W, Sekercioglu et al (2017) A global analysis of traits predicting species sensitivity to habitat fragmentation. Glob Ecol Biogeogr 26:115–127. https://doi.org/10.1111/geb.12509
Khalil H, Hörnfeldt B, Evander M, Magnusson M, Olsson G, Ecke F (2014) Dynamics and drivers of hantavirus prevalence in rodent populations. Vector Borne Zoonotic Dis 14:537–551. https://doi.org/10.1089/vbz.2013.1562
Kittle AM, Watson AC, Chanaka Kumara PH, Nimalka Sanjeewani HK (2012) Status and distribution of the leopard in the central hills of Sri Lanka. Cat News 56:28–31
Kutt AS, Woinarski JCZ (2007) The effects of grazing and fire on vegetation and the vertebrate assemblage in a tropical savanna woodland in northeastern Australia. J Trop Ecol 23:95–106. https://doi.org/10.1017/S0266467406003579
LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci 100:567–571. https://doi.org/10.1073/pnas.0233733100
Martin PS, Gheler-Costa C, Lopes PC, Rosalino LM, Verdade LM (2012) Terrestrial non-volant small mammals in agro-silvicultural landscapes of Southeastern Brazil. For Ecol Manag 282:185–195. https://doi.org/10.1016/j.foreco.2012.07.002
McCauley DJ, Salkeld DJ, Young HS, Makundi R, Dirzo R, Eckerlin RP, Lambin EF, Gaffikin L, Barry M, Helgen KM (2015) Effects of land use on plague (Yersinia pestis) activity in rodents in Tanzania. Am J Trop Med Hyg 92:776–783. https://doi.org/10.4269/ajtmh.14-0504
McShea WJ, Stewart C, Peterson L, Erb P, Stuebing R, Giman B (2009) The importance of secondary forest blocks for terrestrial mammals within an Acacia/secondary forest matrix in Sarawak, Malaysia. Biol Conserv 142:3108–3119. https://doi.org/10.1016/j.biocon.2009.08.009
Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270. https://doi.org/10.1080/10408410902989837
Mills JN (2006) Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Biodiversity 7:9–17. https://doi.org/10.1080/14888386.2006.9712789
Murtaugh PA (2002) Journal quality, effect size, and publication bias in meta-analysis. Ecology 83:1162–1166. https://doi.org/10.1890/0012-9658(2002)083[1162:JQESAP]2.0.CO;2
Ostfeld RS, Holt RD (2004) Are predators good for your health? Evaluating evidence for top-down regulations of zoonotic disease reservoirs. Front Ecol Environ 2:13–20. https://doi.org/10.1890/1540-9295(2004)002[0013:APGFYH]2.0.CO;2
Ostfeld RS, Schauber EM, Canham CD, Kessing F, Jones CG, Wolff JO (2001) Effects of acorn production and mouse abundance on abundance and Borrelia burgdorferi infection prevalence of nymphal Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1:55–63
Payton ME, Greenstone MH, Schenker N (2003) Overlapping confidence intervals or standard error intervals: what do they mean in terms of statistical significance? J Insect Sci 3:34–39. https://doi.org/10.1093/jis/3.1.34
Pimm S (1991) The balance of nature? Ecological issues in the conservation of species and communities. University of Chicago Press, Chicago
Plourde BT, Burgess TL, Eskew EA, Roth TM, Stephenson N, Foley JE (2017) Are disease reservoirs special? Taxonomic and life history characteristics. PLoS One 12:e0180716. https://doi.org/10.1371/journal.pone.0180716
Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Sinauer Associates, Sunderland
Rubio AV, Ávila-Flores R, Suzán G (2014) Responses of small mammals to habitat fragmentation: epidemiological considerations for rodent-borne hantaviruses in the Americas. EcoHealth 11:526–533. https://doi.org/10.1007/s10393-014-0944-9
Singleton GR, Smith AL, Krebs CJ (2000) The prevalence of viral antibodies during a large population fluctuation of house mice in Australia. Epidemiol Infect 125:719–727. https://doi.org/10.1017/s0950268800004945
Taylor LH, Latham SM, Woolhouse MEJ (2001) Risk factors for human disease emergence. Philos Trans R Soc B Biol Sci 356:983–989. https://doi.org/10.1098/rstb.2001.0888
Vanderwel MC, Malcolm JR, Mills SC (2007) A meta-analysis of bird responses to uniform partial harvesting across North America. Conserv Biol 21:1230–1240. https://doi.org/10.1111/j.1523-1739.2007.00756.x
Woinarski JCZ, Rankmore B, Hill B, Griffiths AD, Stewart A, Grace B (2009) Fauna assemblages in regrowth vegetation in tropical open forests of the Northern Territory, Australia. Wildl Res 36:675–690
Young HS, Dirzo R, Helgen KM, McCauley DJ, Billeter SA, Kosoy MY, Osikowicz LM, Salkeld DJ, Young TP, Dittmar K (2014) Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa. Proc Natl Acad Sci 111:7036–7704. https://doi.org/10.1073/pnas.1404958111
Young HS, McCauley DJ, Dirzo R, Nunn CL, Campana MG, Agwanda B et al (2017) Interacting effects of land use and climate on rodent-borne pathogens in Central Kenya. Philos Trans R Soc B 372:20160116. https://doi.org/10.1098/rstb.2016.0116
Funding
This work was supported by FONDECYT 3160037 and CONICYT + PAI Convocatoria Nacional de Subvención a la Instalación en la Academia 2018 No. PAI77180009. HM was supported by a CONACyT MSc scholarship and PAEP-UNAM.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mendoza, H., Rubio, A.V., García-Peña, G.E. et al. Does land-use change increase the abundance of zoonotic reservoirs? Rodents say yes. Eur J Wildl Res 66, 6 (2020). https://doi.org/10.1007/s10344-019-1344-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-019-1344-9