Siberian flying squirrels do not anticipate future resource abundance
Tóm tắt
One way to cope with irregularly occurring resources is to adjust reproduction according to the anticipated future resource availability. In support of this hypothesis, few rodent species have been observed to produce, after the first litter born in spring, summer litters in anticipation of autumn’s seed mast. This kind of behaviour could eliminate or decrease the lag in population density normally present in consumer dynamics. We focus on possible anticipation of future food availability in Siberian flying squirrels, Pteromys volans. We utilise long-term data set on flying squirrel reproduction spanning over 20 years with individuals living in nest-boxes in two study areas located in western Finland. In winter and early spring, flying squirrels depend on catkin mast of deciduous trees. Thus, the temporal availability of food resource for Siberian flying squirrels is similar to other mast-dependent rodent species in which anticipatory reproduction has been observed. We show that production of summer litters was not related to food levels in the following autumn and winter. Instead, food levels before reproduction, in the preceding winter and spring, were related to production of summer litters. In addition, the amount of precipitation in the preceding winter was found to be related to the production of summer litters. Our results support the conclusion that Siberian flying squirrels do not anticipate the mast. Instead, increased reproductive effort in female flying squirrels is an opportunistic event, seized if the resource situation allows.
Tài liệu tham khảo
Boutin S, Wauters LA, McAdam AG, Humphries MM, Tosi G, Dhondt AA. Anticipatory reproduction and population growth in seed predators. Science. 2006;314:1928–30.
Valone TJ. Are animals capable of Bayesian updating? An empirical review. Oikos. 2006;112:252–9.
Raby CR, Alexis DM, Dickinson A, Clayton NS. Planning for the future by western scrub-jays. Nature. 2007;445:919–21.
Railsback SF, Harvey BC. Trait-mediated trophic interactions: is foraging theory keeping up? Trends Ecol Evol. 2013;28:119–25.
Ostfeld RS, Keesing F. Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol. 2000;15:232–7.
Lindström E. Reproductive effort in the red fox, Vulpes vulpes, and future supply of a fluctuating prey. Oikos. 1988;52:115–9.
Jȩdrzejewska B, Jeȩdrzejewski W. Predation in vertebrate communities: the Bialowieza Primeval Forest as a case study. Berlin: Springer-Verlag; 1998.
Lobo N, Millar JS. Indirect and mitigated effects of pulsed resources on the population dynamics of a northern rodent. J Anim Ecol. 2013;82:814–25.
Bogdziewicz M, Zwolak R, Crone EE. How do vertebrates respond to mast seeding? Oikos. 2016;125:300–7.
Wauters LA, Githiru M, Bertolino S, Molinari A, Tosi G, Lens L. Demography of alpine red squirrel populations in relation to fluctuations in seed crop size. Ecography. 2008;31:104–14.
Bergeron P, Réale D, Humphries MM, Garant D. Anticipation and tracking of pulsed resources drive population dynamics in eastern chipmunks. Ecology. 2011;92:2027–34.
Lebl K, Kürbisch K, Bieber C, Ruf T. Energy or information? the role of seed availability for reproductive decisions in edible dormice. J Comp Physiol B. 2010;180:447–56.
Williams CT, Lane JE, Humphries MM, McAdam AG, Boutin S. Reproductive phenology of a food-hoarding mast-seed consumer: resource- and density-dependent benefits of early breeding in red squirrels. Oecologia. 2014;174:777–88.
Selonen V, Varjonen R, Korpimäki E. Immediate or lagged responses of a red squirrel population to pulsed resources. Oecologia. 2015;177:401–11.
White TCR. Mast seeding and mammal breeding: can a bonanza food supply be anticipated? N Z J Zool. 2007;34:179–83.
Ranta H, Hokkanen T, Linkosalo T, Laukkanen L, Bondenstam K, Oksanen A. Male flowering of birch: spatial synchronization, year-to-year variation and relation of catkin numbers and airborne pollen counts. Forest Ecol Manage. 2008;255:643–50.
Ranta H, Oksanen A, Hokkanen T, Bondestam K, Heino S. Masting by Betula-species; applying the resource budget model to north European data sets. Int J Biometeorol. 2005;49:146–51.
White TCR. The role of food, weather and climate in limiting the abundance of animals. Biol Rev. 2008;83:227–48.
Mäkelä A. Liito-oravan, Pteromys volans L. Ravintobiologiasta (feeding biology of flying squirrel, in Finnish). Master’s Thesis, University of Oulu, Finland. 1981.
Mäkelä A. Liito-oravan (Pteromys volans L.) ravintokohteet eri vuodenaikoina ulosteanalyysin perusteella (diet of flying squirrel, in Finnish). Helsinki: WWF Finland Reports 8; 1996. p. 54–8.
Hanski IK, Mönkkönen M, Reunanen P, Stevens PC. Ecology of the Eurasian flying squirrel (Pteromys volans) in Finland. In: Goldingay R, Scheibe J, editors. Biology of gliding mammals. Furth (Germany): Filander; 2000. p. 67–86.
Sulkava P, Sulkava R. Liito-oravan ravinnosta ja ruokailutavoista Keski-Suomessa (feeding habits of flying squirrel; in Finnish). Luonnon tutkija. 1993;97:136–8.
Selonen V, Wistbacka R, Korpimäki E. Food abundance and weather modify reproduction of two arboreal squirrel species. J Mammal. 2016;97:1376–84.
Hanski IK, Selonen V. Female-biased natal dispersal in the Siberian flying squirrel. Behav Ecol. 2009;20:60–7.
Selonen V, Painter JN, Rantala S, Hanski IK. Mating system and reproductive success in the Siberian flying squirrel. J Mammal. 2013;94:1266–73.
Selonen V, Hanski IK, Wistbacka R. Communal nesting is explained by subsequent mating rather than kinship or thermoregulation in the Siberian flying squirrel. Behav Ecol Socio. 2014;68:971–80.
Lampila S, Wistbacka A, Mäkelä A, Orell M. Survival and population growth rate of the threatened Siberian flying squirrel (Pteromys volans) in a fragmented forest landscape. Ecoscience. 2009;16:66–74.
Hokkanen T. Seed crops and seed crop forecasts for a number of tree species. In: Mälkönen E, Babich NA, Krutov VI, Markova IA, editors. Forest regeneration in the northern parts of Europe. Proceedings of the Finnish–Russian forest regeneration seminar in Vuokatti, Finland, Sept 28th–Oct 2nd, 1998. Metsäntutkimuslaitoksen tiedonantoja—The Finnish Forest Research Institute, Research Papers. 2000;790: 87–97.
Rousi M, Heinonen J. Temperature sum accumulation effects on within-population variation and long-term trends in date of bud burst of European white birch (Betula pendula). Tree Physiol. 2007;27:1019–25.
Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. 2nd ed. New York: Springer; 2002.
Post E, Forchhammer MC. Climate change reduces reproductive success of an arctic herbivore through trophic mismatch. Phil Trans Roy Soc Lond B. 2008;363:2369–75.
Eeva T, Veistola S, Lehikoinen E. Timing of breeding in subarctic passerines in relation to food availability. Can J Zool. 2000;78:67–78.
Possen BJHM, Oksanen E, Rousi M, Ruhanen H, Ahonen V, Tervahauta A, Heinonen J, Heiskanen J, Kärenlampi S, Vapaavuori EM. Adaptability of birch (Betula pendula Roth) and aspen (Populus tremula L.) genotypes to different soil moisture conditions. Forest Ecol Manage. 2011;262:1387–99.
Marcello GJ, Wilder SM, Meikle DB. Population dynamics of a generalist rodent in relation to variability in pulsed food resources in a fragmented landscape. J Anim Ecol. 2008;77:41–6.
Kager T, Fietz J. Food availability in spring influences reproductive output in the seed-preying edible dormouse (Glis glis). Can J Zool. 2009;87:555–65.
Smith CC. The coevolution of pine squirrels (Tamiasciurus) and conifers. Ecol Monogr. 1970;40:349–71.
Fletcher QE, Boutin S, Lane JE, LaMontagne JM, McAdam AG, Krebs CJ, Humphries MM. The functional response of a hoarding seed predator to mast seeding. Ecology. 2010;91:2673–83.
LaMontagne JM, Williams CT, Donald JL, Humphries MM, McAdam AG, Boutin S. Linking intraspecific variation in territory size, cone supply, and survival of North American red squirrels. J Mammal. 2013;94:1048–58.
Larsen KW, Becker CD, Boutin S, Blower M. Effects of hoard manipulations on life history and reproductive success of female red squirrels (Tamiasciurus hudsonicus). J Mammal. 1997;78:192–203.
Bieber C. Population dynamics, sexual activity, and reproduction failure in the fat dormouse (Myoxus glis). J Zool. 1998;244:223–9.
Pilastro A, Tavecchia G, Marin G. Long living and reproduction skipping in the fat dormouse. Ecology. 2003;84:1784–92.
Kelly D, Sork VL. Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst. 2002;33:427–47.
Yang LH, Edwards KF, Byrnes JE, Bastow JL, Wright AN, Spence KO. A meta-analysis of resource pulse–consumer interactions. Ecol Monogr. 2010;80:125–51.