Environmental drivers of long-term variations in the abundance of the red hocicudo mouse (Oxymycterus rufus) in Pampas agroecosystems

Abstract

During the 20th century, there has been an ongoing agricultural expansion and global warming, two of the main determinants influencing biodiversity changes in Argentina. The red hocicudo mouse (Oxymycterus rufus) inhabits subtropical grasslands and riparian habitats and has increased its abundance in recent years in central Argentina agroecosystems. This paper describes the long-term temporal changes in O. rufus abundance in Exaltación de la Cruz department, Buenos Aires province, Argentina, in relation to weather fluctuations and landscape features, as well as analyzes the spatio-temporal structure of captures of animals. We used generalized liner models, semivariograms, the Mantel test, and autocorrelation functions for the analysis of rodent data obtained from trappings conducted between 1984 and 2014. O. rufus showed an increase in abundance across the years of study, with its distribution depending on landscape features, such as habitat types and the distance to floodplains. Capture rates showed a spatio-temporal aggregation, suggesting expansion from previously occupied sites. O. rufus was more abundant at lower minimum temperatures in summer, higher precipitation in spring and summer, and lower precipitations in winter. Weather conditions affected O. rufus abundance, but there was local variation that differed from global patterns of climate change.

Keywords

agroecosystems / climate change / linear habitats / Oxymycterus rufus / rodent

References

[1] Alard D, Poudevigne I (2002). Biodiversity in changing landscapes: from species or patch assemblages to system organisation. In: Lewen RSW, Poudevigne I, Teeuw RM, eds. Application of Geographic Information Systems and Remote Sensing in River Studies. Backhuys Publishers, Kerkwerve, The Netherlands, pp. 9–24.

[2] Andreo V, Lima M, Provensal C, Priotto J, Polop J (2009a). Population dynamics of two rodent species in agroecosystems of central Argentina: Intra-specific competition, land-use, and climate effects. Population Ecology 51, 297–306.

[3] Andreo V, Provensal C, Scavuzzo M, Lamfri M, Polop J (2009b). Environmental factors and population fluctuations of Akodon azarae (Muridae, Sigmodontinae) in central Argentina. Austral Ecology 34, 132–42.

[4] Begon M, Townsend J, Harper C (2006). Ecology: From Individuals to Ecosystems, 4th edn. Blackwell, Oxford, UK.

[5] Bellocq MI (1990). Composición y variación temporal de la dieta de Tyto alba en ecosistemas agrarios pampeanos, Argentina. Vida Silvestre Neotropical 2, 32–5.

[6] Bilenca DN (1993). Caracterización de los nichos ecológicos y organización de las comunidades de roedores cricétidos en la Region Pampeana. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[7] Bilenca D, Miñarro F (2004). Identificación de Áreas Valiosas de Pastizal en las Pampas y Campos de Argentina, Uruguay y sur de Brasil, 1st edn. Fundación Vida Silvestre Argentina, Buenos Aires, Argentina.

[8] Bilenca DN, González-Fischer CM, Teta P, Zamero M (2007). Agricultural intensification and small mammal assemblages in agroecosystems of the Rolling Pampas, central Argentina. Agriculture, Ecosystems and Environment 121, 371–5.

[9] Bilenca D, Codesido M, Fischer CG, Carusi LP, Zufiaurre E, Abba A (2012). Impactos de la transformación agropecuaria sobre la biodiversidad en la provincia de Buenos Aires. Revista Del Museo Argentino de Ciencias Naturales 14, 189–98.

[10] Bivand RS, Pebesma EJ, Gomez-Rubio V (2013). Applied Spatial Data Analysis with R, 2nd edn.Springer, New York. https://asdar-book.org/

[11] Bolger DT, Alberts AC, Sauvajot RM et al. (1997). Response of rodents to habitat fragmentation in coastal southern California. Ecological Applications 7, 552–63.

[12] Bonaventura SM, Piantanida MJ, Gurini L, Sanchez Lopez MI (1991). Habitat selection in population of cricetine rodents in the region Delta (Argentina). Mammalia 55, 339–54.

[13] Bonaventura SM, Pancotto V, Madanes N, Vicari R (2003). Microhabitat use and density of sigmodontine rodents in Spartina densiflora freshwater marshes, Argentina. Mammalia 67, 367–77.

[14] Busch M, Kravetz FO (1992a). Competitive interactions among rodents (Akodon azarae, Calomys laucha, C. musculinus and Oligoryzomys flavescens) in a two-habitat system. I. Spatial and numerical relationships. Mammalia 56, 45–56.

[15] Busch M, Kravetz FO (1992b). Competitive interactions among rodents II. Effect of species removal. Mammalia 56, 541–54.

[16] Busch M, Miño MH, Dadon JR, Hodara K (2001). Habitat selection by Akodon azarae and Calomys laucha (Rodentia, Muridae) in pampean agroecosystems. Mammalia 65, 29–48.

[17] Busch M, Bilenca DN, Cittadino EA, Cueto GR (2005). Effect of removing a dominant competitor, Akodon azarae (Rodentia, Sigmodontinae) on community and population parameters of small rodent species in Central Argentina. Austral Ecology 30, 168–78.

[18] Busch M, Hodara K (2010). Uso y selección de habitat y competencia inter específica en roedores sigmodontinos de la región pampeana. In: Polop J, Busch M, eds. Biología y Ecología de Pequenos Roedores en la Región Pampeana de Argentina. Enfoques y Perspectivas. Universidad Nacional de Córdoba, Córdoba, Argentina, pp. 147–71.

[19] Butet A, Leroux ABA (2001). Effects of agriculture development on vole dynamics and conservation of Montagu's harrier in western French wetlands. Biological Conservation 100, 289–95.

[20] Calfayan LM (2016). Variaciones espacio-temporales de la abundancia del ratón hocicudo rojizo (Oxymcterus rufus) en agroecosistemas pampeanos en los últimos 30 años y su vinculación con cambios en variables ambientales. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[21] Cameron GN, Scheel D (2001). Getting warmer: Effect of global climate change on distribution of rodents in Texas. Journal of Mammalogy 82, 652–80.

[22] Camilloni I (2018). Argentina y el cambio climático. Ciencia e Investigación 68, 5–10.

[23] Castellarini F, Provensal C, Polop J (2002). Effect of weather variables on the population fluctuations of muroid Calomys venustus in central Argentina. Acta Oecologica 23, 385–91.

[24] Cavia R (1999). Efecto de las labores agrícolas sobre los pequeños roedores en agroecosistemas pampeanos. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[25] Cittadino EA, De Carli P, Busch M, Kravetz FO (1994). Effects of food supplementation on rodents in winter. Journal of Mammalogy 75, 446–53.

[26] Cittadino EA, Hodara K, Kravetz FO (1997). Dispersión invernal de Oligoryzomys flavescens (Rodentia: Muridae) en bordes de campos de cultivos de agroecosistemas pampeanos. Ecologia Austral 7, 13–9.

[27] Courtalon P (2003). Comparación de la comunidad de roedores sigmodontinos entre parcelas de maíz y soja de agroecosistemas pampeanos. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[28] Cueto VR, Piantanida MJ, Cagnoni M (1995). Population demography of Oxymycterus rufus (Rodentia: Cricetidae) inhabiting a patchy environment of the delta of the Paraná river, Argentina. Acta Theriologica 40, 123–30.

[29] Ellis BA, Mills JN, Childs JE et al. (1997). Structure and floristics of habitats associated with five rodent species in an agroecosystem in Central Argentina. Journal of Zoology 243, 437–60.

[30] Engelthaler DM, Mosley DG, Cheek JE et al. (1999). Climatic and environmental patterns associated with hantavirus pulmonary syndrome, four corners region, United States. Emerging Infectious Diseases 5, 87–94.

[31] Fletcher R, Fortin M (2018). Spatial Ecology and Conservation Modeling, 1st edn. Springer International Publishing, Cham, Switzerland.

[32] Fox J, Weisberg S (2019). An R Companion to Applied Regression, 3rd edn. Sage, Thousand Oaks, CA. https://socialsciences.mcmaster.ca/jfox/Books/Companion/

[33] Fraschina J (2005). Eficiencia de forrajeo de Akodon azarae bajo distintas condiciones de cobertura vegetal y oferta de alimento en bordes de campos de cultivo. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[34] Fraschina J (2011). Efectos de cambios en el uso de la tierra sobre ensambles de roedores en agroecosistemas pampeanos. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[35] Fraschina J, León VA, Busch M (2012). Long-term variations in rodent abundance in a rural landscape of the Pampas, Argentina. Ecological Research 27, 191–202.

[36] Fraschina J, León VA, Busch M (2014). Role of landscape scale in the distribution of rodents in an agroecosystem of Argentina. Journal of Agricultural Science 6, 22–35.

[37] Ghersa CM, Martínez-Ghersa MA, León RJC (1998). Cambios en el paisaje pampeano y sus efectos sobre los sistemas de soporte de la vida. In: Solbrig OT, Vainesman L, eds. Hacia Una Agricultura Productiva y Sostenible En La Pampa. Harvard University and Consejo Profesional de Ingenierı́a Agronómica (CPIA), Buenos Aires, pp. 38–71.

[38] Gomez MD, Coda J, Simone I et al. (2015). Agricultural land-use intensity and its effects on small mammals in the central region of Argentina. Mammal Research 60, 415–23.

[39] Gómez Villafañe IE, Miñarro FO, Valenzuela L, Bilenca DN (2009). Experimental assessment of rodent control on two poultry farms of central Argentina. Journal of Applied Poultry Research 18, 622–9.

[40] Gómez Villafañe IE, Busch M, Fraschina J et al. (2019). Oxymycterus rufus. In: SAyDS–SAREM, ed. Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción. Lista Roja de los mamíferos de Argentina. http://cma.sarem.org.ar

[41] González Fischer CM, Baldi G, Codesido M, Bilenca D (2012). Seasonal variations in small mammal-landscape associations in temperate agroecosystems: A study case in Buenos Aires province, central Argentina. Mammalia 76, 399–406.

[42] González Fischer CM, Cavia R, Picasso P, Bilenca D (2017). Regional and local determinants of rodent assemblages in agroecosystems of the Argentine Pampas. Journal of Mammalogy 98, 1760–7.

[43] Gorosito IL (2018). Ecología y comportamiento de Oligoryzomys flavescens y Akodon azarae en relación con la transmisión de hantavirus. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[44] Guidobono JS (2013). Dinámica poblacional de roedores en agroecosistemas y su relación con variables ambientales. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[45] Guidobono JS, Muñoz J, Muschetto E, Teta P, Busch M (2016). Food habits of geoffroy's cat (Leopardus geoffroyi) in agroecosystem habitats of Buenos Aires, Argentina. Ecologia Austral 26, 40–50.

[46] Guisan A, Thuiller W, Zimmermann NE (2017). Habitat Suitability and Distribution Models: With Applications in R, 1st edn. Cambridge University Press, United Kingdom.

[47] Hartig F (2021). DHARMa: Residual Diagnostics for Dierarchical (Multi-Level /Mixed) Regression Models. Available from URL: https://cran.r-project.org/package=DHARMa

[48] Heroldová M, Bryja J, Zejda J, Tkadlec E (2007). Structure and diversity of small mammal communities in agriculture landscape. Agriculture, Ecosystems and Environment 120, 206–10.

[49] Hetem RS, Fuller A, Maloney SK, Mitchell D (2014). Responses of large mammals to climate change. Temperature 1, 115–27.

[50] Hörnfeldt B, Hipkiss T, Eklund U (2005). Fading out of vole and predator cycles? Proceedings of the Royal Society B: Biological Sciences 272, 2045–9.

[51] Hughes L (2000). Biological consequences of global warming: is the signal already. Trends in Ecology & Evolution 15, 56–61.

[52] IGN (2014). Capas SIG. Instituto Geográfico Nacional. [Cited Dec 2014.] Available from URL: https://www.ign.gob.ar/NuestrasActividades/InformacionGeoespacial/CapasSIG

[53] IPCC (2021). Summary for policymakers. In: Masson-Delmotte V, Zhai P, Pirani A et al., eds. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, pp. 3–32.

[54] Klempa B (2009). Hantaviruses and climate change. Clinical Microbiology and Infection 15, 518–23.

[55] Kravetz FO (1972). Estudio del régimen alimentario, períodos de actividad y otros rasgos ecológicos en una poblacion de “raton hocicudo” Oxymycterus rufus platensis Thomas de Punta Lara. Acta Zoologica Lilloana 29, 201–12.

[56] Kravetz FO, Belloq M, Busch M, Bonaventura SM, Monjeau A (1987). Efecto de la aplicación de un anticuagulante sobre la comunidad de roedores en campos de cultivo. Anales Museo de Historia Natural 18, 153–6.

[57] Kravetz FO, Manjón MC, Busch M, Percich RE, Marconi PN, Torres MP (1981). Ecología de Calomys laucha (Rodentia, Cricetidae) en el Departamento de Río Cuarto (Córdoba). I. Dinámica de población. Ecología 6, 15–22.

[58] Legendre P, Legendre L (2012). Numerical Ecology, 3rd edn. Elsevier Science, Amsterdam.

[59] Lenth RV (2021). Emmeans: Estimated Marginal Means, aka Least-Squares Means. Available from URL: https://cran.r-project.org/package=emmeans

[60] Lima M (2001). The dynamics of natural populations: feedback structures in fluctuating environments. Revista Chilena de Historia Natural 74, 317–29.

[61] Lovera R, Fernández MS, Cavia R (2019). Small rodent species on pig and dairy farms: habitat selection and distribution. Pest Management Science 75, 1234–41.

[62] Lüdecke D (2021). SjPlot: Data Visualization for Statistics in Social Science. Available from URL: https://cran.r-project.org/package=sjPlot

[63] Lüdecke D, Ben-Shachar MS, Patil I, Waggoner P, Makowski D (2021). Performance: An R package for assessment, comparison and testing of statistical models. Journal of Open Source Software 6, 3139.

[64] Manrique V (2000). Evaluación de componentes del fitness en dos especies de roedores (Akodon azarae y Calomys laucha) en un sistema campo-borde de agroecosistemas pampeanos. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires.

[65] Maroli M, Vadell MV, Iglesias AJ, Padula P, Gómez Villafañe IE (2015). Daily movements and microhabitat selection of Hantavirus reservoirs and other sigmodontinae rodent species that inhabit a protected natural area of Argentina. EcoHealth 12, 421–31.

[66] Maroli M, Vadell MV, Padula P, Gómez Villafañe IE (2018). Rodent abundance and hantavirus infection in protected area, east-central Argentina. Emerging Infectious Diseases 24, 131–4.

[67] Maroli M, Gómez Villafañe IE (2021). Urban rodents of the city of Diamante, Entre Ríos, Argentina. Mastozoologia Neotropical 28, e0542.

[68] Maroli M, Burgos EF, Piña CI, Gómez Villafañe IE (2022). Population survey of small rodents on islands located inside a region of endemism for hantavirus pulmonary syndrome. Journal of Mammalogy 103, 209–20.

[69] Martínez-Ghersa MA, Ghersa CM (2005). Consecuencias de los recientes cambios agrícolas. Ciencia Hoy 15, 37–45.

[70] Mason-Romo ED, Ceballos G, Lima M, Martínez-Yrízar A, Jaramillo VJ, Maass M (2018). Long-term population dynamics of small mammals in tropical dry forests, effects of unusual climate events, and implications for management and conservation. Forest Ecology and Management 426, 123–33.

[71] Massa C, Teta P, Cueto GR (2014). Effects of regional context and landscape composition on diversity and composition of small rodent assemblages in Argentinian temperate grasslands and wetlands. Mammalia 78, 371–82.

[72] Matteucci S (2012). Ecorregión Pampa. In: Morello J, Matteucci S, Rodriguez A, Silva M, eds. Ecorregiones y Complejos Ecosistémicos Argentinos. Orientación Gráfica Editora S.R.L., Buenos Aires, Argentina, pp. 391–446.

[73] Meserve PL, Kelt DA, Previtali MA, Milstead WB, Gutiérrez JR (2011). Global climate change and small mammal populations in north-central Chile. Journal of Mammalogy 92, 1223–35.

[74] Mills JN, Ellis BA, McKee KT, Maiztegui JI, Childs JE (1991). Habitat associations and relative densities of rodent populations in cultivated areas of central Argentina. Journal of Mammalogy 72, 470–9.

[75] Miño M, Cavia R, Gómez Villafañe IE, Bilenca DN, Cittadino EA, Busch M (2001). Estructura y diversidad de dos comunidades de pequeños roedores en agroecosistemas de la provincia de Buenos Aires, Argentina. Boletín de la Sociedad de Biología de Concepción Chile 72, 73–81.

[76] Moritz C, Patton JL, Conroy CJ, Parra JL, White GC, Beissinger SR (2008). Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322, 261–4.

[77] Muschetto E, Cueto GR, Cavia R, Padula PJ, Suárez OV (2018). Long-term study of a Hantavirus reservoir population in an urban protected area, Argentina. Eco-Health 15, 804–14.

[78] NOAA (2014). Multivariate ENSO Index Version 2 (MEI.v2). National Oceanic and Atmosferic Administration. [Cited March 2016.] Available from URL: https://www.esrl.noaa.gov/psd/enso/mei/

[79] Oksanen J, Blanchet FG, Friendly M et al. (2020). Vegan: Community Ecology Package. R Package Version 2.5-6. 2019. Available from URL: https://cran.r-project.org/package=vegan

[80] Pardiñas UFJ, Teta P, D'Elía G (2010). Roedores sigmodontinos de la región pampeana: historia evolutiva, sistemática y taxonomía. In: Polop JJ,Busch M, eds. Biología y Ecologia de Pequeños Roedores en la Región Pampeana Argentina: Enfoques y Perspectivas. Universidad Nacional de Córdoba, Cordoba, pp. 9–36.

[81] Paruelo JM, Guerschman JP, Verón SR (2005). Expansión agrícola y cambios en el uso del suelo. Ciencia Hoy 15, 14–23.

[82] QGIS Development Team (2018). QGIS Geographic Information System. Open Source Geospatial Foundation Project. Available from URL: http://qgis.osgeo.org

[83] Quinn GP, Keough MJ (2002). Experimental Design and Data Analysis for Biologists, 1st edn. Cambridge University Press, Cambridge, United Kingdom.

[84] R Core Team (2020). R: A Language and Environment for Statistical Computing. Available from URL: https://www.r-project.org/

[85] Robinson GR, Holt RD, Gaines MS et al. (1992). Diverse and contrasting effects of habitat fragmentation. Science 257, 524–6.

[86] Roccatagliata J (2013). Los ferrocarriles en la Argentina, 1st edn. EUDEBA, Buenos Aires, Argentina.

[87] Royama T (1992). Analytical Population Dynamics, 1st edn. Chapman and Hall, London, UK.

[88] Sala OE, Stuart Chapin F, Armesto JJ et al. (2000). Global biodiversity scenarios for the year 2100. Science 287, 1770–4.

[89] Sarkar D (2008). Lattice: Multivariate data visualization with R. Springer. Available from URL: http://lmdvr.r-forge.r-project.org

[90] SIGA (2014). Datos históricos. Sistema de Información y Gestión Agrometeorológica. [Cited Dec 2014.] Available from URL: http://siga.inta.gob.ar/#/data

[91] SMN (2022a). Anomalías de Precipitación y Temperatura Asociadas. Servicio Meteorológico Nacional. [Cited Dec 2021.] Available from URL: https://www.smn.gob.ar/como_nos_afecta

[92] SMN (2022b). Estadísticas de largo plazo. Servicio Meteorológico Nacional. [Cited Dec 2021.] Available from URL: https://www.smn.gob.ar/estadisticas

[93] Soriano A, León R, Sala O et al. (1991). Río de la Plata grasslands. In: Coupland R, ed. Ecosystems of the World 8A. Natural Grasslands. Introduction and Western Hemisphere. Elsevier, Amsterdam, The Netherlands, pp. 367–407

[94] Suárez OV (1994). Diet and habitat selection of Oxymycterus rutilans (Rodentia, Cricetidae). Mammalia 58, 225–34.

[95] TCNCC (2015). Resumen Ejecutivo de la Tercera Comunicación Nacional de la República Argentina a la Convención Marco de las Naciones Unidas sobre el Cambio Climático. Secretaría de Ambiente y Desarrollo Sustentable, 264. Available from URL: https://www.argentina.gob.ar/ambiente/cambio-climatico/tercera-comunicacion

[96] Teta P, Laponte D, Acosta A (2004). Sigmodontinos (Mammalia, Rodentia) del Holoceno tardío del nordeste de la provincia de Buenos Aires (Argentina). Mastozoología Neotropical 11, 69–80.

[97] Teta P, González-Fischer CM, Codesido M, Bilenca DN (2010). A contribution from Barn Owl pellets analysis to known micromammalian distributions in Buenos Aires province, Argentina. Mammalia 74, 97–103.

[98] Teta P, Hercolini C, Cueto G (2012). Variation in the diet of Western Barn Owls (Tyto alba) along an urban-rural gradient. Wilson Journal of Ornithology 124, 589–96.

[99] Teta P, Formoso A, Tammone M et al. (2014). Micromamíferos, cambio climático e impacto antrópico: ¿Cuánto han cambiado las comunidades del sur de América del Sur en los últimos 500 años? Therya 5, 7–38.

[100] Vadell MV, Gómez Villafañe IE (2016). Environmental variables associated with Hantavirus reservoirs and other small rodent species in two National Parks in the Paraná delta, Argentina: Implications for disease prevention. EcoHealth 13, 248–60.

[101] Venables WN, Ripley BD (2002). Modern Applied Statistics with S, 4th edn. Springer, New York. http://www.stats.ox.ac.uk/pub/MASS4/

[102] Viglizzo EF, Lértora F, Pordomingo AJ, Bernardos JN, Roberto ZE, Del Valle H (2001). Ecological lessons and applications from one century of low external-input farming in the pampas of Argentina. Agriculture, Ecosystems and Environment 83, 65–81.

[103] Zuleta GA, Kravetz FO, Busch M, Percich RE (1988). Dinámica poblacional del ratón del pastizal pampeano (Akodon azarae) en ecosistemas agrarios de Argentina. Revista Chilena de Historia Natural 61, 231–44.

[104] Zuur AF, Ieno EN, Walker NJ et al. (2009). Mixed Effects Models and Extensions in Ecology with R, Vol. 574. Springer, New York.

[105] Zuur AF, Ieno EN, Elphick CS (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.

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.