Abstract
Understanding how species respond to disturbance in human-modified ecosytems is critical for management and conservation of biodiversity in the Anthropocene. In agroecosystems, human disturbances severely modify the habitat of species, particularly for those that live in burrows. The common vole Microtus arvalis (Pallas, 1778) is a semi-fossorial microtine, which often exhibits large abundance fluctuations, becoming an agricultural pest in peak years. We evaluated how both agrarian disturbances (via types of crop and their management) and landscape heterogeneity influenced the abundance of common vole burrow systems along a yearly cycle, at the field and landscape scales. We seasonally recorded the number of burrows and their recent occupation in circular plots of 200-m radius including different types of crops in intensified agrarian landscapes in NW Spain. Our results showed a marked seasonal and spatial pattern in both total abundance and abundance of occupied burrows. After a population peak year, only 31% of burrows were occupied across the year (from 41% in spring–summer to 12% in autumn). The crop type and its management in relation to soil disturbance were the main factors driving seasonal and spatial dynamics of burrow abundance at the field and landscape scale. Alfalfa fields held the highest abundance of both total and occupied burrow systems across the year, while fields of traditional-tilled cereal retained the lowest. As a result, at the landscape scale, plots with a greater surface devoted to traditional cereal crops maintained a lower relative number of burrow systems. Regarding the landscape structural heterogeneity, plots with longer length of field margins and lower area of watercourses maintained higher abundance of burrow systems. An adequate landscape-scale planning of crop types, agricultural practices, and distribution of non-crop habitats could be a promising sustainable method to reduce the risk of crop-damaging vole plagues.
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Bates D, Maechler M, Bolker BM, Walker S (2015a) lme4: linear mixed-effects models using “Eigen” and S4. R package version 1.1-10
Bates D, Maechler M, Bolker BM, Walker S (2015b) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bohdal T, Navrátil J, Sedláček F (2016) Small terrestrial mammals living along streams acting as natural landscape barriers. Ekológia Bratisl 35:191–204. https://doi.org/10.1515/eko-2016-0015
Bonnet T, Crespin L, Pinot A, Bruneteau L, Bretagnolle V, Gauffre B (2013) How the common vole copes with modern farming: insights from a capture–mark–recapture experiment. Agric Ecosyst Environ 177:21–27. https://doi.org/10.1016/j.agee.2013.05.005
Bowman J, Forbes GJ, Dilworth TG (2001) The spatial component of variation in small-mammal abundance measured at three scales. Can J Zool 79:137–144. https://doi.org/10.1139/cjz-79-1-137
Bradbury RB, Payne RJH, Wilson JD, Krebs JR (2001) Predicting population responses to resource management. Trends Ecol Evol 16:440–445. https://doi.org/10.1016/S0169-5347(01)02189-9
Briner T, Nentwig W, Airoldi J-P (2005) Habitat quality of wildflower strips for common voles (Microtus arvalis) and its relevance for agriculture. Agric Ecosyst Environ 105:173–179. https://doi.org/10.1016/j.agee.2004.04.007
Bring J (1994) How to standardize regression coefficients. Am Stat 48:209–213. https://doi.org/10.2307/2684719
Brown PR, Huth NI, Banks PB, Singleton GR (2007) Relationship between abundance of rodents and damage to agricultural crops. Agric Ecosyst Environ 120:405–415. https://doi.org/10.1016/j.agee.2006.10.016
Brügger A, Nentwig W, Airoldi J-P (2010) The burrow system of the common vole (M. arvalis, Rodentia) in Switzerland. Mammalia 74. https://doi.org/10.1515/mamm.2010.035
Cavia R, Villafañe IEG, Cittadino EA, Bilenca DN, Miño MH, Busch M (2005) Effects of cereal harvest on abundance and spatial distribution of the rodent Akodon azarae in central Argentina. Agric Ecosyst Environ 107:95–99. https://doi.org/10.1016/j.agee.2004.09.011
Crawley MJ (2007) The R book. John Wiley ans Sons, Chichester. UK
de Redon L, Machon N, Kerbiriou C, Jiguet F (2010) Possible effects of roadside verges on vole outbreaks in an intensive agrarian landscape. Mamm Biol - Z Für Säugetierkd 75:92–94. https://doi.org/10.1016/j.mambio.2009.02.001
Delattre P, Giraudoux P, Baudry J, Musard P, Toussaint M, Truchetet D, Stahl P, Poule ML, Artois M, Damange JP, Quéré JP (1992) Land use patterns and types of common vole (Microtus arvalis) population kinetics. Agric Ecosyst Environ 39:153–168. https://doi.org/10.1016/0167-8809(92)90051-C
Delattre P, Giraudoux P, Baudry J, Quéré JP, Fichet E (1996) Effect of landscape structure on common vole (Microtus arvalis) distribution and abundance at several space scales. Landsc Ecol 11:279–288. https://doi.org/10.1007/BF02059855
Delattre P, Giraudoux P, Damange J-P, Quere J-P (1990) Recherche d’un indicateur de la cinétique démographique des populations du campagnol des champs (Microtus arvalis). Rev D'ecologie 45:375–384
Delattre P, Morellet N, Codreanu P, Miot S, Quéré JP, Sennedot F, Baudry J (2009) Influence of edge effects on common vole population abundance in an agricultural landscape of eastern France. Acta Theriol (Warsz) 54:51–60. https://doi.org/10.1007/BF03193137
Donald PF, Green RE, Heath MF (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc R Soc Lond B Biol Sci 268:25–29. https://doi.org/10.1098/rspb.2000.1325
Eggert J, Wolff C, Richter K (2011) Searching for alternative methods for a sustainable population management of the common vole (Microtus arvalis). In: Julius-Kühn-Archiv. Book of abstracts, 8th European Vertebrate Pest Management Conference, Berlin, p 154-155
Epstein PR (1995) Emerging diseases and ecosystem instability: new threats to public health. Am J Public Health 85:168–172
Fargallo JA, Martínez-Padilla J, Viñuela J, Blanco G, Torre I, Vergara P, de Neve L (2009) Kestrel-prey dynamic in a Mediterranean region: the effect of generalist predation and climatic factors. PLoS One 4:e4311. https://doi.org/10.1371/journal.pone.0004311
Fischer C, Schröder B (2014) Predicting spatial and temporal habitat use of rodents in a highly intensive agricultural area. Agric Ecosyst Environ 189:145–153. https://doi.org/10.1016/j.agee.2014.03.039
Fischer C, Thies C, Tscharntke T (2011) Small mammals in agricultural landscapes: opposing responses to farming practices and landscape complexity. Biol Conserv 144:1130–1136. https://doi.org/10.1016/j.biocon.2010.12.032
Fox J, Weisberg S (2011) An {R} Companion to applied regression, Second Edition. Sage, Thousand Oaks (CA)
Gaines MS, Vivas AM, Baker CL (1979) An experimental analysis of dispersal in fluctuating vole populations: demographic parameters. Ecology 60:814–828. https://doi.org/10.2307/1936617
Gratz NG (2018) Rodents and human disease: a global appreciation. In: Rodent pest management. CRC Press, Boca Raton, pp 111–180
Heroldová M, Michalko R, Suchomel J, Zejda J (2018) Influence of no-tillage versus tillage system on common vole (Microtus arvalis) population density. Pest Manag Sci n/a-n/a 74:1346–1350. https://doi.org/10.1002/ps.4809
Heroldová M, Tkadlec E, Bryja J, Zejda J (2008) Wheat or barley?: Feeding preferences affect distribution of three rodent species in agricultural landscape. Appl Anim Behav Sci 110:354–362. https://doi.org/10.1016/j.applanim.2007.05.008
Heroldová M, Zejda J, Zapletal M et al (2004) Importance of winter rape for small rodents. Plant Soil Environ 50:175–181
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Hygnstrom SE, VerCauteren KC, Hines RA, Mansfield CW (2000) Efficacy of in-furrow zinc phosphide pellets for controlling rodent damage in no-till corn. Int Biodeterior Biodegrad 45:215–222
Hyndman R, Bergmeir C, Caceres G, et al (2018) Forecast: forecasting functions for time series and linear models. R package version 8.3. http://pkg.robjhyndman.com/forecast
Hyndman RJ, Khandakar Y (2008) Automatic time series forecasting: the forecast package for R. J Stat Softw 27. https://doi.org/10.18637/jss.v027.i03
Jacob J (2003) Short-term effects of farming practices on populations of common voles. Agric Ecosyst Environ 95:321–325. https://doi.org/10.1016/S0167-8809(02)00084-1
Jacob J, Brown JS (2000) Microhabitat use, giving-up densities and temporal activity as short- and long-term anti-predator behaviors in common voles. Oikos 91:131–138. https://doi.org/10.1034/j.1600-0706.2000.910112.x
Jacob J, Hempel N (2003) Effects of farming practices on spatial behaviour of common voles. J Ethol 21:45–50
Jacob J, Manson P, Barfknecht R, Fredricks T (2014) Common vole (Microtus arvalis) ecology and management: implications for risk assessment of plant protection products: common voles in the risk assessment of plant protection products. Pest Manag Sci 70:869–878. https://doi.org/10.1002/ps.3695
Jacob J, Tkadlec E (2010) Rodent outbreaks in Europe: dynamics and damage. In: Singleton GR, Belmain S, Brown PR (eds) Rodent outbreaks: ecology and impacts. International Rice Research Institute, Los Baños, Philippines, pp 207–223
Jánová E, Heroldová M (2016) Response of small mammals to variable agricultural landscapes in Central Europe. Mamm Biol - Z Für Säugetierkd 81:488–493. https://doi.org/10.1016/j.mambio.2016.06.004
Jánová E, Heroldová M, Bryja J (2008) Conspicuous demographic and individual changes in a population of the common vole in a set-aside alfalfa field. Ann Zool Fenn 45:39–54. https://doi.org/10.5735/086.045.0104
Jánová E, Heroldová M, Konecny A, Bryja J (2011) Traditional and diversified crops in South Moravia (Czech Republic): habitat preferences of common vole and mice species. Mamm Biol - Z Für Säugetierkd 76:570–576. https://doi.org/10.1016/j.mambio.2011.04.003
Jánová E, Heroldová M, Nesvadbová J, Bryja J, Tkadlec E (2003) Age variation in a fluctuating population of the common vole. Oecologia 137:527–532. https://doi.org/10.1007/s00442-003-1379-0
Jareño D, Viñuela J, Luque-Larena JJ, Arroyo L, Arroyo B, Mougeot F (2014) A comparison of methods for estimating common vole (Microtus arvalis) abundance in agricultural habitats. Ecol Indic 36:111–119. https://doi.org/10.1016/j.ecolind.2013.07.019
Jareño D, Viñuela J, Luque-Larena JJ, Arroyo L, Arroyo B, Mougeot F (2015) Factors associated with the colonization of agricultural areas by common voles Microtus arvalis in NW Spain. Biol Invasions 17:2315–2327. https://doi.org/10.1007/s10530-015-0877-4
Kinlaw A (1999) A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 41:127–145. https://doi.org/10.1006/jare.1998.0476
Krebs CJ (2013) Population fluctuations in rodents. In: University of Chicago Press. Chicago, USA
Lantová P, Lanta V (2009) Food selection in Microtus arvalis: the role of plant functional traits. Ecol Res 24:831–838. https://doi.org/10.1007/s11284-008-0556-3
Laundré JW, Reynolds TD (1993) Efects of soil structure on burrow characteristic of five small mammal species. Gt Basin Nat 4:358–366
Leu ST, Kappeler PM, Bull CM (2010) Refuge sharing network predicts ectoparasite load in a lizard. Behav Ecol Sociobiol 64:1495–1503. https://doi.org/10.1007/s00265-010-0964-6
Liro A (1974) Renewal of burrows by the common vole as the indicator of its numbers. Acta Theriol (Warsz) 19:259–272
Luque-Larena JJ, Mougeot F, Arroyo B, Vidal MD, Rodríguez-Pastor R, Escudero R, Anda P, Lambin X (2017) Irruptive mammal host populations shape tularemia epidemiology. PLoS Pathog 13:e1006622. https://doi.org/10.1371/journal.ppat.1006622
Luque-Larena JJ, Mougeot F, Roig DV, Lambin X, Rodríguez-Pastor R, Rodríguez-Valín E, Anda P, Escudero R (2015) Tularemia outbreaks and common vole (Microtus arvalis) irruptive population dynamics in northwestern Spain, 1997–2014. Vector-Borne Zoonotic Dis 15:568–570. https://doi.org/10.1089/vbz.2015.1770
Mackin-Rogalska R (1979) Elements of the spatial organization of a common vole population. Acta Theriol (Warsz) 24:171–199
Mackin-Rogalska R, Adamczewska-Andrzejwsika K, Nabaglo L (1986) Common vole numbers in relation to the utilization of burrow systems. Acta Theriol (Warsz) 31:17–44
Madejón E, Murillo JM, Moreno F, López MV, Arrue JL, Alvaro-Fuentes J, Cantero C (2009) Effect of long-term conservation tillage on soil biochemical properties in Mediterranean Spanish areas. Soil Tillage Res 105:55–62. https://doi.org/10.1016/j.still.2009.05.007
MAGRAMA (2012) Encuesta sobre Superficies y Rendimientos de Cultivos 2012. Ministerio de Agricultura, Alimentación y Medio Ambiente. Secretaría General Técnica. Centro de Publicaciones
MAGRAMA (2015) Encuesta sobre Superficies y Rendimientos de Cultivos 2015. Ministerio de Agricultura, Alimentación y Medio Ambiente. Secretaría General Técnica. Centro de Publicaciones
Marques SF, Rocha RG, Mendes ES, Fonseca C, Ferreira JP (2015) Influence of landscape heterogeneity and meteorological features on small mammal abundance and richness in a coastal wetland system, NW Portugal. Eur J Wildl Res 61:749–761. https://doi.org/10.1007/s10344-015-0952-2
McLaughlin A, Mineau P (1995) The impact of agricultural practices on biodiversity. Agric Ecosyst Environ 55:201–212. https://doi.org/10.1016/0167-8809(95)00609-V
Millán de la Peña NM, Butet A, Delettre Y et al (2003) Response of the small mammal community to changes in western French agricultural landscapes. Landsc Ecol 18:265–278
Moreno S, Kufner MB (1988) Seasonal patterns in the wood mouse population in Mediterranean scrubland. Acta Theriol (Warsz) 33:79–85
Nowak RM (ed) (1999) Walker’s mammals of the world, 6th edn. Johns Hopkins University Press, Baltimore
Oñate JJ, Suárez F, Peco B et al (2003) Programa Piloto de Acciones de Conservación de la Biodiversidad en Sistemas Ambientales con Usos Agrarios en el Marco del Desarrollo Rural. Informe Final. Direccion General de Conservación de la Naturaleza. Secretaría General de Medio Ambiente. Ministerio de Medio Ambiente, Madrid
Paz A, Jareño D, Arroyo L, Viñuela J, Arroyo B, Mougeot F, Luque-Larena JJ, Fargallo JA (2013) Avian predators as a biological control system of common vole (Microtus arvalis) populations in north-western Spain: experimental set-up and preliminary results. Pest Manag Sci 69:444–450. https://doi.org/10.1002/ps.3289
Pinot A, Gauffre B, Bretagnolle V (2014) The interplay between seasonality and density: consequences for female breeding decisions in a small cyclic herbivore. BMC Ecol 14:17. https://doi.org/10.1186/1472-6785-14-17
Quantum GIS Development Team (2015) Qgis. Quantum GIS development team
Reichman OJ, Smith SC (1990) Burrows and burrowings behavior in mammals. In: Current Mammalogy. Plenum Press, New York and London
Revelle W (2016) Package “psych” version 1.6.6. Psych: procedures for psychological, psychometric, and personality research. https://cran.r-project.org/web/packages/psych/index.html
Rodríguez-Pastor R, Luque-Larena JJ, Lambin X, Mougeot F (2016) “Living on the edge”: the role of field margins for common vole (Microtus arvalis) populations in recently colonised Mediterranean farmland. Agric Ecosyst Environ 231:206–217. https://doi.org/10.1016/j.agee.2016.06.041
Roos D, Caminero Saldaña C, Arroyo B, Mougeot F, Luque-Larena JJ, Lambin X (2019) Unintentional effects of environmentally-friendly farming practices: arising conflicts between zero-tillage and a crop pest, the common vole (Microtus arvalis). Agric Ecosyst Environ 272:105–113. https://doi.org/10.1016/j.agee.2018.11.013
Rosário IT, Mathias ML (2004) Annual weight variation and reproductive cycle of the wood mouse (Apodemus sylvaticus) in a Mediterranean environment. Mammalia 68:133–140
R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Shannon CE (1948) A mathematical theory of communication. Part I, Part II Bell Syst Tech J 27:623–656
Singleton GR, Belmain S, Brown PR, Hardy B (eds) (2010) Rodent outbreaks: ecology and impacts. International Rice Research Institute, Los Baños, Philippines
Sokolova NA, Sokolov AA, Ims RA, Skogstad G, Lecomte N, Sokolov VA, Yoccoz NG, Ehrich D (2014) Small rodents in the shrub tundra of Yamal (Russia): density dependence in habitat use? Mamm Biol - Z Für Säugetierkd 79:306–312. https://doi.org/10.1016/j.mambio.2014.04.004
Sousa WP (1984) The role of disturbance in natural communities. Annu Rev Ecol Syst 15:353–391
Sterner RT, Petersen BE, Gaddis SE, Tope KL, Poss DJ (2003) Impacts of small mammals and birds on low-tillage, dryland crops. Crop Prot 22:595–602. https://doi.org/10.1016/S0261-2194(02)00236-3
Terraube J, Arroyo B, Madders M, Mougeot F (2011) Diet specialisation and foraging efficiency under fluctuating vole abundance: a comparison between generalist and specialist avian predators. Oikos 120:234–244. https://doi.org/10.1111/j.1600-0706.2010.18554.x
Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci 96:5995–6000. https://doi.org/10.1073/pnas.96.11.5995
Turner MG (2010) Disturbance and landscape dynamics in a changing world1. Ecology 91:2833–2849. https://doi.org/10.1890/10-0097.1
Vidal D, Alzaga V, Luque-Larena JJ, Mateo R, Arroyo L, Viñuela J (2009) Possible interaction between a rodenticide treatment and a pathogen in common vole (Microtus arvalis) during a population peak. Sci Total Environ 408:267–271. https://doi.org/10.1016/j.scitotenv.2009.10.001
White PS, Pickett STA (1985) Chapter 1 - natural disturbance and patch dynamics: an introduction. In: The ecology of natural disturbance and patch dynamics. Academic Press, San Diego, pp 3–13
Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397
Witmer G, Sayler R, Huggins D, Capelli J (2007) Ecology and management of rodents in no-till agriculture in Washington, USA. Integr Zool 2:154–164. https://doi.org/10.1111/j.1749-4877.2007.00058.x
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgments
We are very grateful to Luis M. Carrascal and Javier Seoane for statistical advice and workers of GREFA and students of Universidad Autónoma de Madrid for help during censuses. Special thanks to Iván García Egea, Silvia Herrero Cófreces, Alfonso Paz Luna, Daniel Jareño Gómez, Ana Benítez López, María Calero Riestra, and Jorge Piñeiro Álvarez for their help during fieldwork. We would like to also thank the numerous landowners who allowed us access to their property.
Funding
This study was funded by I+D National Plan Projects of the Spanish Ministry of Economy, Industry and Competitiveness (CGL2011-30274 and CGL2015-71255-P), and the Fundación BBVA Research Project TOPIGEPLA (2014 call).
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Santamaría, A.E., Olea, P.P., Viñuela, J. et al. Spatial and seasonal variation in occupation and abundance of common vole burrows in highly disturbed agricultural ecosystems. Eur J Wildl Res 65, 52 (2019). https://doi.org/10.1007/s10344-019-1286-2
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DOI: https://doi.org/10.1007/s10344-019-1286-2