Abstract
In this work, we examined the relationship of Oligoryzomys longicaudatus’ (the Andes virus [ANDV] host, commonly known as the colilargo) occupancy and the cover of dominant woody and herbaceous plant species recorded in censuses along traplines for mice. We found that O. longicaudatus occupancy probability increased with high percentages of Rosa rubiginosa, Plantago lanceolata, Rumex acetosella, and Holcus lanatus, while it decreased with an increased cover of Mulinum spinosum and Ochetophila trinervis. The four positively related species are exotic plants. R. rubiginosa, the most conspicuous one, is capable of invading all types of habitats and forms dense shrublands in the ecotone between forest and steppe. These results are partly consistent with diet studies indicating that sweet briar fruits are the main item consumed by colilargos. The relationship of the ANDV main host with such an invasive plant poses a likely increased ANDV transmission risk to local communities making use of sweet briar’s fruits. We discuss further implications of this problem in relation to hantavirus epidemiology in southern Argentina.
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Data availability
The datasets used during the current study are available at: https://github.com/veroandreo/colilargos-sweetbriar
References
Alonso DO, Iglesias A, Coelho R, Periolo N, Bruno A, Córdoba MT, Filomarino N, Quipildor M, Biondo E, Fortunato E, Bellomo C, Martínez VP (2019) Epidemiological description, case-fatality rate, and trends of hantavirus pulmonary syndrome: 9 years of surveillance in Argentina. J Med Virol 91:1173–1181. https://doi.org/10.1002/jmv.25446
Andreo V (2012) Variables ambientales en la dinámica espacial de Oligoryzomys longicaudatus (Huésped Del Virus Andes) en la región Noroeste de Chubut, Argentina, PhD. Universidad Nacional de Río Cuarto, Río Cuarto, Argentina
Andreo V, Provensal C, Levis S, Pini N, Enría D, Polop J (2012) Summer-autumn distribution and abundance of the hantavirus host, Oligoryzomys longicaudatus, in northwestern Chubut, Argentina. J Mammal 93:1559–1568. https://doi.org/10.1644/11-MAMM-A-201.1
Cabrera A, Willink A (1973) Biogeografía de América Latina, vol 13. Programa Regional de Desarrollo Científico y Tecnológico. Departamento de Asuntos Científicos, Secretaria General de la Organización de los Estados Americanos
Cantoni G, Padula P, Calderon G, Mills J, Herrero E, Sandoval P, Martinez V, Pini N, Larrieu E (2001) Seasonal variation in prevalence of antibody to hantaviruses in rodents from southern Argentina. Trop Med Int Health 6:811–816. https://doi.org/10.1046/j.1365-3156.2001.00788.x
Damascos M, Gallopin G (1992) Ecología de un arbusto introducido (Rosa rubiginosa L. = Rosa eglanteria L.): Riesgo de invasión y efectos en las comunidades vegetales de la región andino-patagónica de Argentina. Rev Chil Hist Nat 65:395–407
Dorazio RM, Royle JA (2005) Estimating size and composition of biological communities by modeling the occurrence of species. J Am Stat Assoc 100:389–398. https://doi.org/10.1198/016214505000000015
Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–472. https://doi.org/10.1214/ss/1177011136
Gonzalez-Ittig R, Salazar-Bravo J, Polop J, Gardenal CN (2008) Isolation and characterization of microsatellite markers in Oligoryzomys longicaudatus (Muridae, Sigmodontinae, Oryzomini), the natural reservoir of genotype Andes hantavirus. Mol Ecol Resour 8:1466–1468. https://doi.org/10.1111/j.1755-0998.2008.02231.x
Herrera I, Goncalves E, Pauchard A, Bustamante RO (2016) Manual de Plantas Invasoras de Sudamérica. Trama Impresores S.A, Chile
Holt RD, Pacala SW, Smith TW, Liu J (1995) Linking contemporary vegetation models with spatially explicit animal population models. Ecol Appl 5:20–27
INDEC (2010) Instituto Nacional de Estadística y Censos. Censo Nacional de Población, Hogares y Viviendas
Johnson MD, De León YL (2015) Effect of an invasive plant and moonlight on rodent foraging behavior in a coastal dune ecosystem. PLoS One 10(2):e0117903. https://doi.org/10.1371/journal.pone.0117903
Juan E, Levis S, Pini N, Polop J, Steinmann AR, Provensal MC (2019) Mechanisms of hantavirus transmission in Oligoryzomys longicaudatus. EcoHealth 16:671–681. https://doi.org/10.1007/s10393-019-01454-y
Kellner K (2016) jagsui: a wrapper around 'RJAGS' to streamline 'JAGS' analyses. R package version 1.4. 4. https://CRAN.R-project.org/package=jagsUI.
Kéry M, Royle JA (2016) Applied hierarchical modeling in ecology: analysis of distribution, abundance and species richness in R and BUGS, prelude and static models, vol 1. Elsevier Inc, New York
Larrieu E, Herrero E, Labanchi JL, Padula P (2003) Seroprevalencia de hantavirus en roedores y casos humanos en el sur de la Argentina. Rev Bras Epidemiol 6:68–75
Levis S, Morzunov SP, Rowe JE, Enria D, Pini N, Calderon G, Sabattini M, St Jeor SC (1998) Genetic diversity and epidemiology of hantaviruses in Argentina. J Infect Dis 177:529–538. https://doi.org/10.1086/514221
Loss SR, Noden BH, Fuhlendorf SD (2022) Woody plant encroachment and the ecology of vector-borne diseases. J Appl Ecol 59(2):420–430. https://doi.org/10.1111/1365-2664.14083
Lozada M, Guthmann N, Baccala N (2000) Microhabitat selection of five sigmodontine rodents in a forest-steppe transition zone in northwestern Patagonia. Stud Neotrop Fauna Environ 35:85–90. https://doi.org/10.1076/0165-0521(200008)35:2;1-9;FT085
Mack R, Smith M (2011) Invasive plants as catalysts for the spread of human parasites. NeoBiota 9:13–29. https://doi.org/10.3897/neobiota.9.1156
Martinez VP, Bellomo CM, Cacace ML, Suárez P, Bogni L, Padula P (2010) Hantavirus pulmonary syndrome in Argentina, 1995-2008. Emerg Infect Dis 16:1853–1860
Meserve P, Kelt D, Milstead W, Gutiérrez J (2003) Thirteen years of shifting top-down and bottom-up control. BioScience 53:633–646. https://doi.org/10.1641/0006-3568(2003)053[0633:TYOSTA]2.0.CO;2
Mills J, Childs JE, Ksiazek TG, Peters CJ, Velleca WM (1995) Methods for trapping and sampling small mammals for virologic testing. United States Department of Health and Human Services, Atlanta, Georgia
Ministerio de Salud y Desarrollo Social (2019) Boletín Integrado de Vigilancia. Semana 4. www.argentina.gob.ar/sites/default/files/biv_437_semanal.pdf Accessed 21 January 2020.
Monjeau JA, Birney EC, Ghermandi L, Sikes RS, Phillips CJ (1998) Plants, small mammals, and the hierarchical landscape classifications of Patagonia. Landsc Ecol 13:285–306. https://doi.org/10.1023/A:1008012613305
Morrison M, Marcot B, Mannan W (2006) Wildlife-habitat relationships. Concepts and Applications, 3rd edn. Island Press, Washington DC
Murúa R, González L (1982) Microhabitat selection in two Chilean cricetid rodents. Oecologia 52:12–15
Padula P, Edelstein A, Miguel SD, López NM, Rossi CM, Rabinovich RD (1998) Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241:323–330. https://doi.org/10.1006/viro.1997.8976
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. J Wildl Dis 48(2):267–281. https://doi.org/10.7589/0090-3558-48.2.267
Pardiñas U, Teta P, Cirignoli S, Podesta D (2003) Micromamíferos (Didelphimorphia y Rodentia) de Norpatagonia extra Andina, Argentina: Taxonomía alfa y Biogeografía. Mastozoologia Neotrop 10:69–113
Piudo L, Monteverde M, González Capria S, Padula P, Carmanchahi P (2005) Distribution and abundance of sigmodontine rodents in relation to hantavirus in Neuquén, Argentina. J Vector Ecol 30:119–125
Piudo L, Monteverde M, Walker RS, Douglass RJ (2011) Rodent community structure and Andes virus infection in sylvan and peridomestic habitats in northwestern Patagonia, Argentina. Vector-Borne Zoonotic Dis 11:315–324. https://doi.org/10.1089/vbz.2009.0242
Polop F, Provensal C, Pini N, Levis S, Priotto J, Costa F, Polop J, Enría D (2010) Temporal and spatial host abundance and prevalence of Andes hantavirus in southern Argentina. EcoHealth 7:176–184. https://doi.org/10.1007/s10393-010-0333-y
Polop F, Juan E, Polop J, Provensal C (2014a) Spatial and temporal variation of terrestrial rodent assemblages in Cholila, Chubut province, Argentina. Stud Neotrop Fauna Environ 49:151–157. https://doi.org/10.1080/01650521.2014.947075
Polop F, Sepúlveda L, Pelliza Sbriller A, Polop J, Provensal C (2014b) Food habits of Oligoryzomys longicaudatus (Rodentia) in a steppe-forest transitional area of Argentinean Patagonia. Ecol Austral 24:304–310. https://doi.org/10.25260/EA.14.24.3.0.7
Polop F, Sepúlveda L, Pelliza Sbriller A, Polop J (2015) Estructura de la dieta de los roedores sigmodontinos en los arbustales del ecotono. Mastozoología Neotrop 22:85–95
R Core Team (2018) R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria www.R-project.org/
Rotenberry JT (1985) The role of habitat in avian community composition: physiognomy or floristics? Oecologia 67:213–217. https://doi.org/10.1007/BF00384286
Rotenberry JT, Wiens JA (1998) Foraging patch selection by shrub-steppe sparrows. Ecology 79:1160–1173. https://doi.org/10.1890/0012-9658(1998)079[1160:FPSBSS]2.0.CO;2
Royle J, Dorazio R (2008) Hierarchical modeling and inference in ecology: the analysis of data from populations, metapopulations and communities. Elsevier Inc, New York
Sikes RS, the Animal Care and Use Committee of the American Society of Mammalogists (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97:663–688. https://doi.org/10.1093/jmammal/gyw078
Somlo R, Cohen L (1997) Tablas de valor nutritivo de especies forrajeras patagónicas. 1. Cordillera-Precordillera. Comunicación Técnica N°5. INTA-EEA S.C. de Bariloche. 13 pp.
Tammone MN, Lacey EA, Pardiñas UF (2020) Dramatic recent changes in small mammal assemblages from Northern Patagonia: a caution for paleoenvironmental reconstructions. Holocene 30(11):1579–1590. https://doi.org/10.1177/0959683620941096
Thompson CM, Gese EM (2013) Influence of vegetation structure on the small mammal community in a shortgrass prairie ecosystem. Acta Theriol 58(1):55–61. https://doi.org/10.1007/s13364-012-0098-5
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14(7):702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Vitousek PM, D'antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21(1):1–16
Zhang S, Isermann M, Gan W, Breed M (2018) Invasive Rosa rugosa populations outperform native populations, but some populations have greater invasive potential than others. Sci Rep 8:5735. https://doi.org/10.1038/s41598-018-23974-3
Acknowledgements
The authors would like to thank Fabian Argel, Bruno San Martin, Francisco Polop, Marcos Torres, Blanca San Martin, Gabriel Martin, and Patricia Codesal for their assistance in different aspects of fieldwork and the identification of plants and mice. We would also like to thank James Mills for kindly reviewing the English language.
Code availability
The scripts used in the current study are available at:https://github.com/veroandreo/colilargos-sweetbriar.
Funding
This work was supported by the Fondo para la Investigación Científica y Tecnológica (FONCyT - PICT/2004 N° 20757), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), and Fundación Mundo Sano (https://www.mundosano.org/en/) from Argentina.
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MCP, JP, and VA designed the study, VA performed the rodent sampling, VA and VH performed the plant sampling, VH identified plants, FC performed the statistical analysis, and FC, VA, and MCP wrote the manuscript. All authors approved the final version.
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Communicated by: Thales Renato Ochotorena de Freitas
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Appendix S1.
Full list of plant species recorded on censuses carried out in the North West of Chubut province (Argentina), 2007–2009 (PDF 108 kb)
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Contreras, F., Andreo, V., Hechem, V. et al. Colilargo’s occupancy and the role of native and exotic plants in hantavirus expansion and transmission risk. Mamm Res 68, 167–176 (2023). https://doi.org/10.1007/s13364-023-00671-9
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DOI: https://doi.org/10.1007/s13364-023-00671-9