Reproductive potential of a vole pest (Arvicola scherman) in Spanish apple orchards

Aitor Somoano, Marcos Miñarro, Jacint Ventura


Fossorial water voles, Arvicola scherman, feed on tree roots causing important damages in European apple orchards. Since the intensity of crop damage produced by rodents ultimately depends on their inherent capacity to increase their population, the main goal of this study was to determine the reproductive potential of the subspecies A. scherman cantabriae in apple orchards from Asturias (NW Spain), where voles breed over the whole year. Our results were compared with those reported for the subspecies A. scherman monticola from the Spanish Pyrenees (where reproduction ceases in winter). Sexual characteristics, body condition, relative age class and number of embryos were recorded from 422 females caught in apple orchards along two years. We found pregnant females all along the year, which were able to produce a high number of litters per year (7.30) although litter size was relatively moderate (first year: 3.87 embryos/female; second year: 3.63 embryos/females). The potential number of pups per female and year (first year: 28.25; second year: 26.50) was substantially higher than that reported for Pyrenean voles, what is probably related with differences in the length of the breeding season and in life histories between subspecies. In our population, the number of implanted embryos correlated positively with the body condition of the mother. Our results reveal that management efforts should not be seasonal as they used to be so far and invite to explore the physiological consequences of management practices.


Arvicola scherman cantabriae; body condition; litter size; reproduction; rodent pest; fossorial water voles

Full Text:



Airoldi JP, 1976. Le terrier de la forme fouisseuse du campagnol terrestre, Arvicola terrestris scherman Shaw (Mammalia, Rodentia). Zeitschrift für Säugetierkunde 41: 23-42.

Airoldi JP, 1978. Etude par capture et recapture d'une population de campagnols terrestres Arvicola terrestris scherman Shaw. Terre et Vie 32: 3-45.

Blake BH, 1982. Reproduction in captive water voles, Arvicola terrestris. J Zool 198: 524-529.

Blant M, Ducommun A, Beuret B, Poitry R, Joseph E, 2009. Influence du paysage et du sol sur les pullulations du campagnol terrestre dans le Jura suisse. Revue Suisse d'Agriculture 41: 301-307.

BOE, 2008. Royal decree 409/2008, of 28 March, that established national program for controlling pests of field voles. Boletín Oficialdel Estado (Spain) No. 86: 19217-19219.

Bronson MT, 1979. Altitudinal variation in the life history of the golden-mantled ground squirrel (Spermophilus lateralis). Ecology 60: 272-279.

Cerqueira D, De Sousa B, Gabrion C, Giraudoux P, Quéré JP, Delattre P, 2006. Cyclic changes in the population structure and reproductive pattern of the water vole, Arvicola terrestris Linnaeus, 1758. Mammalian Biology / Zeitschrift für Säugetierkunde 71: 193-202.

Coeurdassier M, Riols R, Decors A, Mionnet A, David F, Quintaine T, Truchetet D, Scheifler R, Giraudoux P, 2014. Unintentional wildlife poisoning and proposals for sustainable management of rodents. Conserv Biol 28: 315-321.

Defaut R, Note P, Chabalier C, Couval G, Truchetet D, 2009. Expérimentations rodenticides et méthodes alternatives. In: Le campagnol terrestre. Prévention et contrôle des populations, Delattre P, Giraudoux P (eds.). pp: 143-153. Éditions Quæ, Versailles Cedex.

Delattre P, Giraudoux P, 2009. Le campagnol terrestre. Prévention et contrôle des populations. Éditions Quæ, Versailles Cedex. 263 pp.

Díaz M, Alonso CL, 2003. Wood mouse Apodemus sylvaticus winter food supply: density, condition, breeding, and parasites. Ecology 84: 2680-2691.

Díaz-González TE, Fernández-Prieto JA, 2005. Prados y pastos cantábricos: origen y diversidad. In: Producciones agroganaderas: Gestión eficiente y conservación del medio natural; De la Roza B, Martínez A, Carballal A (eds.). pp: 699-730. Vol. II. XLV Reunión Científica de la SEEP, SERIDA, Gijón.

Doonan TJ, Slade NA, 1995. Effects of supplemental food on population dynamics of cotton rats, Sigmodon hispidus. Ecology 76: 814-826.

Dunmire WW, 1960. An altitudinal survey of reproduction in Peromyscus maniculatus. Ecology 41: 174-182.

Eifler MA, Slade NA, Doonan TJ, 2003. The effect of supplemental food on the growth rates of neonatal, young, and adult cotton rats (Sigmodon hispidus) in north eastern Kansas, USA. Acta Oecologica 24: 187-193.

Emlen JT, Davis DE, 1948. Determination of reproductive rates in rat populations by examination of carcasses. Physiol Zool 21: 59-65.

EU, 2010. Directive 2010/63/EU Horizontal Legislation on the Protection of Animal Used for Scientific Purposes. Official Journal of European Union L 276/33-276/79.

Evsikov VI, Skorova SV, Nazarova GG, Moshkin MP, 1989. Photoperiod effect on growth and reproductive functions in water vole (Arvicola terrestris L.). Ekologiya 6: 58-63.

Evsikov VI, Nazarova GG, Muzyka VY, 2008. Body condition and reproductive characteristics of female water voles (Arvicola terrestris L.). Russ J Ecol 39: 414-417.

Fischer D, Imholt C, Pelz HJ, Wink M, Prokop A, Jacob J, 2013. The repelling effect of. plant secondary metabolites on water voles, Arvicola amphibius. Pest Manage Sci 69: 437-443.

Hamar M, Marin D, 1962. Zur Biologie von Arvicola terrestris scherman Shaw 1801 in Rumänien. Travaux du Muséum d'Histoire Naturelle "Grigore Antipa" 3: 401-421.

Hansen TF, Stenseth NC, Henttonen H, 1999. Multiannual vole cycles and population regulation during long winters: an analysis of seasonal density dependence. The American Naturalist 154: 129-139.

Hille SM, Rödel HG, 2014. Small-scale altitudinal effects on reproduction in bank voles. Mammalian Biology 79: 90-95.

INDUROT, 2010. Cartografía del manzano en el Principado de Asturias. Consejería de Medio Rural y Pesca. Gobierno del Principado de Asturias, Mieres, Spain.

Innes DG, 1978. A reexamination of litter size in some North American microtines. Can J Zool 56: 1488-1496.

Isakova GK, Nazarova GG, Evsikov VI, 2012. Early embryonic mortality in the water vole (Arvicola terrestris L.). Russ J Develop Biol 43: 244-247.

Jacob J, 2008. Response of small rodents to manipulations of vegetation height in agro‐ecosystems. Integrative Zoology 3: 3-10.

Jacob J, 2013. Vertebrate pest management: science and application. Pest Manage Sci 69: 321-322.

Jacob J, Hinds LA, Singleton GR, Sutherland DR, Ylönen H, 2007. Is the reproductive potential of wild house mice regulated by extrinsic or intrinsic factors? Austr Ecol 32: 202-209.

Kminiak M, 1968. Einige Bermerkungen zur Population dynamik der Grossen Wühlmaus (Arvicola terrestris L., 1758) in der Jahren 1965 und 1966 in der Sudwestliche Slowakei. Biológia 23: 894-900.

Koskela E, Jonsson P, Hartikainen T, Mappes T, 1998. Limitation of reproductive success by food availability and litter size in the bank vole, Clethrionomys glareolus. Proc R Soc Lond B: Biol Sci 265: 1129-1134.

Kratochvil J, 1974. Vermehrungsfähigkeit der Art Arvicola terrestris (L.) in der CSSR (Mamm. Microtidae). Zoologicke Listy 23: 3-17.

Maksimov AA, 1959. Reproduction and fluctuation of the water vole in landscapes of Western Siberia. Vodní. krysa i borba s něj Z. Sib. Novosibirsk 71-120.

Mappes T, Koskela E, Ylonen H, 1995. Reproductive costs and litter size in the bank vole. Proc R Soc Lond B: Biol Sci 261: 19-24.

Meylan A, 1977. Fossorial forms of the water vole, Arvicola terrestris (L.), in Europe. EPPO Bull 7: 209-218.

Miñarro M, 2012. Weed communities in apple orchards under organic and conventional fertilization and tree-row management. Crop Prot 39: 89-96.

Miñarro M, Montiel C, Dapena E, 2012. Vole pests in apple orchards: use of presence signs to estimate the abundance of Arvicola terrestris cantabriae and Microtus lusitanicus. J Pest Sci 85: 477-488.

Montaz J, Jacquot M, Coeurdassier M, 2014. Scavenging of rodent carcasses following simulated mortality due to field applications of anticoagulant rodenticide. Ecotoxicology 23: 1671-1680.

Morel J, 1981. Le campagnol terrestre, Arvicola terrestris (L.) en Suisse: biologie et systématique (Mammalia, Rodentia). Thèse de Doctorat, Univ. Lausanne, Lausanne, Switzerland.

Morilhat C, Bernard N, Bournais C, Meyer C, Lamboley C, Giraudoux P, 2007. Responses of Arvicola terrestris scherman populations to agricultural practices, and to Talpa europaea abundance in eastern France. Agr Ecosyst Environ 122: 392-398.

Murie JO, Boag DA, Kivett VK, 1980. Litter size in Columbian ground squirrels (Spermophilus columbianus). J Mammal 61: 237-244.

Musser GG, Carleton MC, 2005. Arvicola Lacépède, 1799; Arvicola amphibius (Linnaeus, 1758); Arvicola scherman (Shaw, 1801). In: Mammal species of the world. A taxonomic and geographic reference, 3rd edn; Wilson DE, Reeder DM (eds.). pp: 963-966. Johns Hopkins University Press, Baltimore.

Nazarova GG, Evsikov VI, 2008. Effect of mother's physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole Arvicola terrestris. Russ J Develop Biol 39: 100-107.

Ostfeld RS, 1985. Limiting resources and territoriality in Microtine rodents. American Naturalist 126: 1-15.

Panteleyev PA, 1968. Population ecology of the water vole (English translation of AS Colley, edited by DM Stoddart, 1971). National Lending Library, Boston, Yorkshire, UK.

Pascal M, 1981. Resultats preliminaires de l'etude de la biologie du campagnol terrestre (Arvicola terrestris) dans le Doubs. Defense des Vegetaux 208: 121-134.

Pelikán J, 1972. Arvicola terrestris (L.) indexes of reproduction in Czechoslovakia. Acta Sci Nat Brno 11: 1-50.

Perry JS, 1943. Reproduction in the water‐vole, Arvicola amphibius Linn. Proc Zool Soc Lond 112: 118-130.

Ranchelli E, Barfknecht R, Capizzi D, Riga F, Mazza V, Dell'Agnello F, Zaccaroni M, 2016. From biology to management of Savi's pine vole (Microtus savii): a review. Pest Manage Sci 72: 857-863.

Rattner BA, Lazarus RS, Elliott JE, Shore RF, van den Brink N, 2014. Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife. Environ Sci Technol 48: 8433-8445.

Rivas-Martínez S, Rivas-Sáenz S, 2015. Worldwide bioclimatic classification system. Phytosociological Research Centre. Accessed 4 March 2016.

Saucy F, 2002. Dispersal as a key issue in the biological control of small mammals. Berichte aus der Biologische Bundesanstalt für Land- un Forstwirtschaft 104: 18-27.

Saucy F, Schneiter B, 1998. Juvenile dispersal in the vole, Arvicola terrestris, during rainy nights: a preliminary report. Bulletin de la Société Vaudoise des Sciences Naturelles 84: 333-345.

Smith MH, McGinnis JT, 1968. Relationships of latitude, altitude, and body size to litter size and mean annual production of offspring in Peromyscus. Res Popul Ecol 10: 115-126.

Solonen T, 2006. Overwinter population change of small mammals in southern Finland. Annales Zoologici Fennici 43: 295-302.

Spencer AW, Steinhoff HW, 1968. An explanation of geographic variation in litter size. J Mammal 49: 281-286.

Stoddart DM, 1971. Breeding and survival in a population of water voles. J Anim Ecol 40: 487-494.

Tkadlec E, Zejda J, 1998. Small rodent population fluctuations: the effects of age structure and seasonality. Evol Ecol 12: 191-210.

Tupikova NV, Švecov JG, 1956. Reproduction of the water vole in the Volga-Akhtubinskarea. Zoologicheskii Zhurnal 35: 130-140.

Ventura J, 1993. Crecimiento relativo de Arvicola terrestris monticola (Rodentia, Arvicolidae). Miscellània Zoològica 17: 237-248.

Ventura J, Gosálbez J, 1989. Taxonomic review of Arvicola terrestris (Linnaeus, 1758) (Rodentia, Arvicolidae) in the Iberian Peninsula. Bonner Zoologische Beiträge 40: 227-242.

Ventura J, Gosálbez J, 1990a. Reproduction cycle of Arvicola terrestris (Rodentia, Arvicolidae) in the Aran Valley, Spain. Zeitschrift für Säugetierkunde 55: 383-391.

Ventura J, Gosálbez J, 1990b. Reproduction potential of Arvicola terrestris (Mammalia, Rodentia) in the Northeast of the Iberian Peninsula. Zoologischer Anzeiger 225: 45-54.

Ventura J, Gosálbez J, 1992. Criterios para la determinación de la edad relativa en Arvicola terrestris monticola (Rodentia, Arvicolidae). Miscelània Zoològica 16: 197-206.

Ventura J, Gosálbez J, Lopez-Fuster MJ, 1991. Structure de population d'Arvicola terrestris (Linnaeus, 1758) (Rodentia, Arvicolidae) du Nord - Est Ibérique. Mammalia 55: 85-90.

Walther B, Fuelling O, 2010. Vole trapping fences-a new approach to migration barriers. Proc 14th Int Conf on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing. pp: 341-345. Hohenheim, Germany.

Walther B, Fuelling O, Malevez J, Pelz HJ, 2008. How expensive is vole damage? Proc 13th Int Conf on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing. pp: 330-334. Weinsberg, Germany.

Wiebold JL, Becker WC, 1987. Inequality in function of the right and left ovaries and uterine horns of the mouse. J Reprod Fertil 79: 125-134.

Wieland H, 1973. Beitrag zur Biologie und zum Massenwechsel der Grossen Wühlmaus (Arvicola terrestris L.). Zoologisches Jahrbuch, Systematik 100: 351-428.

Wijngaarden A van, 1954. Biologie en bestrijding von de Woelrat, Arvicola terrestris terrestris (L.) in Nederland. Med Nr 123 Plantenziektenkundige Dienst Wageningen.

Williams CT, Barnes BM, Kenagy GJ, Buck CL, 2014. Phenology of hibernation and reproduction in ground squirrels: integration of environmental cues with endogenous programming. J Zool 292: 112-124.

Yakovleva TV, Bazhan NM, Makarova EN, 1997. Effects of food deprivation in early pregnancy on the development of ovaries and adrenals in female progeny of the water vole (Arvicola terrestris). Comp Biochem Phys C 116: 103-109.

Yuzhik EI, Proskurnyak LP, Nazarova GG, 2015. Correlations of reproductive indices of water vole females (Arvicola amphibius) with morphometric and hormonal characteristics. J Evol Biochem Physiol 51: 139-144.

Zammuto RM, Millar JS, 1985. Environmental predictability, variability, and Spermophilus columbianus life history over an elevational gradient. Ecology 66: 1784-1794.

DOI: 10.5424/sjar/2016144-9870