Abstract
The reproduction of many species is determined by seasonally-driven resource supply. But it is difficult to quantify whether the fecundity is sensitive to short- or long-term exposure to environmental conditions such as rainfall that drive resource supply. Using 25 years of data on individual fecundity of European female rabbits, Oryctolagus cuniculus, from semiarid Australia, we investigate the role of individual body condition, rainfall and temperature as drivers of seasonal and long-term and population-level changes in fecundity (breeding probability, ovulation rate, embryo survival). We built distributed lag models in a hierarchical Bayesian framework to account for both immediate and time-lagged effects of climate and other environmental drivers, and possible shifts in reproduction over consecutive seasons. We show that rainfall during summer, when rabbits typically breed only rarely, increased breeding probability immediately and with time lags of up to 10 weeks. However, an earlier onset of the yearly breeding period did not result in more overall reproductive output. Better body condition was associated with an earlier onset of breeding and higher embryo survival. Breeding probability in the main breeding season declined with increased breeding activity in the preceding season and only individuals in good body condition were able to breed late in the season. Higher temperatures reduce breeding success across seasons. We conclude that a better understanding of seasonal dynamics and plasticity (and their interplay) in reproduction will provide crucial insights into how lagomorphs are likely to respond and potentially adapt to the influence of future climate and other environmental change.
Similar content being viewed by others
References
Aars J, Ims RA (2002) Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles. Ecology 83:3449–3456. doi:10.2307/3072093
Albon SD, Mitchell B, Staines BW (1983) Fertility and body weight in female red deer: a density-dependent relationship. J Anim Ecol 52:969–980. doi:10.2307/4467
Almon S (1965) The distributed lag between capital appropriations and expenditures. Econometrica 33:178–196. doi:10.2307/1911894
Ashworth CJ, Toma LM, Hunter MG (2009) Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos Trans R Soc Lond B 364:3351–3361. doi:10.1098/rstb.2009.0184
Aubry P et al (2012) Monitoring population size of mammals using a spotlight-count-based abundance index: how to relate the number of counts to the precision? Ecol Ind 18:599–607. doi:10.1016/j.ecolind.2012.01.019
Benton TG, Plaistow SJ, Coulson TN (2006) Complex population dynamics and complex causation: devils, details and demography. Proc R Soc Lond B 273:1173–1181. doi:10.1098/rspb.2006.3495
Bolker BM et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi:10.1016/j.tree.2008.10.008
Brambell FWR (1942) Intra-uterine mortality of the wild rabbit, Oryctolagus cuniculus (L). Proc R Soc Lond B 130:462–479. doi:10.1098/rspb.1942.0013
Bronson FH (1985) Mammalian reproduction: an ecological perspective. Biol Reprod 32:1–26. doi:10.1095/biolreprod32.1.1
Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philos Trans R Soc Lond B 364:3331–3340. doi:10.1098/rstb.2009.0140
Carter JO, Hall WB, Brook KD, McKeon GM, Day KA, Paull CJ (2000) Aussie GRASS: Australian grassland and rangeland assessment by spatial simulation. Applications of seasonal climate forecasting in agricultural and natural ecosystems: the Australian experience. In: Hammer GL, Nicholls N, Mitchell C (eds) Applications of seasonal climate forecasting in agricultural and natural ecosystems. Springer, Dordrecht, pp 329–349
Conaway CH, Baskett TS, Toll JE (1960) Embryo resorption in the swamp rabbit. J Wildl Manag 24:197–202. doi:10.2307/3796746
Cooke BD (1974) Food and other resources of the wild rabbit Oryctolagus cuniculus. PhD dissertation, University of Adelaide, Adelaide
Cooke BD (1983) Changes in the age-structure and size of populations of wild rabbits in South Australia, following the introduction of European rabbit fleas, Spilopsyllus cuniculi (Dale), as vectors of myxomatosis. Austral Wildl Res 10:105–120
Cooke B (1990) Rabbit burrows as environments for European Rabbit Fleas, Spilopsyllus-cuniculi (Dale), in Arid South-Australia. Aust J Zool 38:317–325. doi:10.1071/ZO9900317
Cooke BD (2014) Daily food intake of free-ranging wild rabbits in semiarid South Australia. Wildl Res 41:141–148. doi:10.1071/WR14003
Coulson T et al (2001) Age, sex, density, winter weather, and population crashes in soay sheep. Science 292:1528–1531. doi:10.1126/science.292.5521.1528
CSIRO, Australian Bureau of Meteorology (2014) State of the climate. http://www.bom.gov.au/state-of-the-climate/
Dellaportas P, Forster J, Ntzoufras I (2002) On Bayesian model and variable selection using MCMC. Stat Comput 12:27–36. doi:10.1023/a:1013164120801
Desy EA, Thompson CF (1983) Effects of supplemental food on a Microtus pennsylvanicus population in central Illinois. J Anim Ecol 52:127–140. doi:10.2307/4592
Dudzinski M, Mykytowycz R (1961) The eye lens as an indicator of age in the wild rabbit in Australia. Wildl Res 6:156–159. doi:10.1071/CWR9610156
Ebling FJP, Barrett P (2008) The regulation of seasonal changes in food intake and body weight. J Neuroendocrinol 20:827–833. doi:10.1111/j.1365-2826.2008.01721.x
Etterson MA et al (2011) Modeling fecundity in birds: conceptual overview, current models, and considerations for future developments. Ecol Model 222:2178–2190. doi:10.1016/j.ecolmodel.2010.10.013
Fordham DA, Akçakaya HR, Araújo MB, Brook BW (2012a) Modelling range shifts for invasive vertebrates in response to climate change. In: Brodie J, Post E, Doak D (eds) Wildlife conservation in a changing climate. University of Chicago Press, Chicago, pp 86–108
Fordham DA et al (2012b) European rabbit survival and recruitment are linked to epidemiological and environmental conditions in their exotic range. Austral Ecol 37:945–957. doi:10.1111/j.1442-9993.2011.02354.x
Gasparrini A, Armstrong B, Kenward MG (2010) Distributed lag non-linear models. Stat Med 29:2224–2234. doi:10.1002/sim.3940
Gelman A, Meng XL, Stern H (1996) Posterior predictive assessment of model fitness via realized discrepancies. Stat Sin 6:733–760
Gilbert N et al (1987) Comparative dynamics of Australasian rabbit populations. Aust Wildl Res 14:491–503
Hamel S, Gaillard J-M, Yoccoz NG, Loison A, Bonenfant C, Descamps S (2010) Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations. Ecol Lett 13:915–935. doi:10.1111/j.1461-0248.2010.01478.x
Hanski I, Henttonen H, Korpimäki E, Oksanen L, Turchin P (2001) Small-rodent dynamics and predation. Ecology 82:1505–1520. doi:10.2307/5465
Henke SE, Demarais S (1990) Effect of diet on condition indices in black-tailed jackrabbits. J Wildl Dis 26:28–33. doi:10.7589/0090-3558-26.1.28
Hone JIM, Clutton-Brock TH (2007) Climate, food, density and wildlife population growth rate. J Anim Ecol 76:361–367. doi:10.1111/j.1365-2656.2006.01200.x
Jeffrey SJ, Carter JO, Moodie KB, Beswick AR (2001) Using spatial interpolation to construct a comprehensive archive of Australian climate data. Environ Model Softw 16:309–330. doi:10.1016/S1364-8152(01)00008-1
Jonzén N, Pople T, Knape J, Sköld M (2010) Stochastic demography and population dynamics in the red kangaroo Macropus rufus. J Anim Ecol 79:109–116. doi:10.1111/j.1365-2656.2009.01601.x
Kokko H, Lindström J (1998) Seasonal density dependence, timing of mortality, and sustainable harvesting. Ecol Model 110:293–304
Korpimäki E, Brown PR, Jacob J, Pech RP (2004) The puzzles of population cycles and outbreaks of small mammals solved? Bioscience 54:1071–1079
Lambin X, Yoccoz NG (2001) Adaptive precocial reproduction in voles: reproductive costs and multivoltine life-history strategies in seasonal environments. J Anim Ecol 70:191–200. doi:10.1046/j.1365-2656.2001.00494.x
Lindström J, Kokko H (2002) Cohort effects and population dynamics. Ecol Lett 5:338–344. doi:10.1046/j.1461-0248.2002.00317.x
Lof ME, Reed TE, McNamara JM, Visser ME (2012) Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction. Proc R Soc Lond B 279:3161–3169. doi:10.1098/rspb.2012.0431
Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17:551–557. doi:10.1016/s0169-5347(02)02633-2
Minot CS, Taylor EB (1905) Normal plates of the development of the rabbit (Lepus cuniculus). In: Keibel F (ed) Normentafeln zur Entwicklungsgeschichte der Wirbeltiere. Gustav Fischer, Jena
Mutze GJ (2009) Changes in body condition and body size affect breeding and recruitment in fluctuating house mouse populations in south-eastern Australia. Austral Ecol 34:278–293. doi:10.1111/j.1442-9993.2008.01929.x
Mutze G, Bird P, Kovaliski J, Peacock D, Jennings S, Cooke B (2002) Emerging epidemiological patterns in rabbit haemorrhagic disease, its interaction with myxomatosis, and their effects on rabbit populations in South Australia. Wildl Res 29:577–590. doi:10.1071/wr00100
Mutze GJ, Sinclair RG, Peacock DE, Capucci L, Kovaliski J (2014) Is increased juvenile infection the key to recovery of wild rabbit populations from the impact of rabbit haemorrhagic disease? Eur J Wildl Res 60:489–499. doi:10.1007/s10344-014-0811-6
Myers K (1970) The rabbit in Australia. In: Boer PJ, Gradwell GR (eds) Dynamics of populations. Proceedings of the advanced Study Institute on “Dynamics of numbers in populations”, Oosterbeek, The Netherlands
Myers K, Poole WE (1963) A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. V. Population dynamics. Wildl Res 8:166–203. doi:10.1071/CWR9630166
Newey S, Thirgood S (2004) Parasite-mediated reduction in fecundity of mountain hares. Proc R Soc Lond B 271:S413–S415. doi:10.1071/CWR9630166
O’Hara RB, Sillanpää MJ (2009) A review of Bayesian variable selection methods: what, how and which. Bayesian Anal 4:85–117. doi:10.1214/09-ba403
Plard F, Yoccoz NG, Bonenfant C, Klein F, Warnant C, Gaillard J-M (2015) Disentangling direct and growth-mediated influences on early survival: a mechanistic approach. J Anim Ecol 84:1363–1372. doi:10.1111/1365-2656.12378
Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Proceedings of the 3rd international workshop on Distributed Statistical Computing R Project for statistical computing, Vienna, Austria
Rödel HG et al (2005) Timing of breeding and reproductive performance of female European rabbits in response to winter temperature and body mass. Can J Zool 83:935–942. doi:10.1139/z05-084
Roxburgh SH et al (2004) A critical overview of model estimates of net primary productivity for the Australian continent. Funct Plant Biol 31:1043–1059. doi:10.1071/FP04100
Royle JA (2004) N-mixture models for estimating population size from spatially replicated counts. Biometrics 60:108–115
Sæther BE, Tufto J, Engen S, Jerstad K, Røstad OW, Skåtan JE (2000) Population dynamical consequences of climate change for a small temperate songbird. Science 287:854–856. doi:10.1126/science.287.5454.854
Schwartz J (2000) The distributed lag between air pollution and daily deaths. Epidemiology 11:320–326. doi:10.1097/00001648-200005000-00016
Stockley P (2003) Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc R Soc Lond B 270:271–278. doi:10.1098/rspb.2002.2228
Swihart RK (1984) Body size, breeding season length, and life history tactics of lagomorphs. Oikos 43:282–290. doi:10.2307/3544145
Thompson PM, Ollason JC (2001) Lagged effects of ocean climate change on fulmar population dynamics. Nature 413:417–420. doi:10.1038/35096558
Via S, Gomulkiewicz R, Dejong G, Scheiner SM, Schlichting CD, Vantienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217. doi:10.1016/s0169-5347(00)89061-8
von Holst D, Hutzelmeyer H, Kaetzke P, Khaschei M, Rödel HG, Schrutka H (2002) Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behav Ecol Sociobiol 51:245–254. doi:10.1007/s00265-001-0427-1
Wells K, Dolich T, Wahl J, O’Hara RB (2013) Spatio-temporal dynamics in waterbirds during the non-breeding season: effects of local movements, migration and weather are monthly, not yearly. Basic Appl Ecol 14:523–531. doi:10.1016/j.baae.2013.07.001
Wells K, Lakim MB, O’Hara RB (2014) Shifts from native to invasive small mammals across gradients from tropical forest to urban habitat in Borneo. Biodivers Conserv 23:2289–2303. doi:10.1007/s10531-014-0723-5
Wells K et al (2015) Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics. J R Soc Interface 12:20141184. doi:10.1098/rsif.2014.1184
Welty LJ, Peng RD, Zeger SL, Dominici F (2009) Bayesian distributed lag models: estimating effects of particulate matter air pollution on daily mortality. Biometrics 65:282–291. doi:10.1111/j.1541-0420.2007.01039.x
West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413:628–631. doi:10.1038/35098076
Zellweger-Fischer J, Kery M, Pasinelli G (2011) Population trends of brown hares in Switzerland: the role of land-use and ecological compensation areas. Biol Conserv 144:1364–1373. doi:10.1016/j.biocon.2010.11.021
Acknowledgments
We thank D. Chinner, B. Sutton, F. Anderson and F. Bartholomaeus for technical assistance in the field and laboratory; and R. Sinclair, D. Peacock, E. Roy-Dufresne, M. Lurgi and A. Jones for various discussions. Comments from N. Yoccoz and an anonymous reviewer helped to improve an earlier draft of the paper. Australian Research Council Grants (LP12020024, FT140101192) supported K.W. and D.A.F. The Biodiversity and Climate Research Centre funded R.B.O’H. through the Landesoffensive zur Entwicklung wissenschaftlich-ökonomischer Exzellenz.
Author contribution statement
BC conceived and designed the field experiments. KW, RBO’H, TAAP, DAF performed the analysis. All authors contributed to writing the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Janne Sundell.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wells, K., O’Hara, R.B., Cooke, B.D. et al. Environmental effects and individual body condition drive seasonal fecundity of rabbits: identifying acute and lagged processes. Oecologia 181, 853–864 (2016). https://doi.org/10.1007/s00442-016-3617-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3617-2