Timing and Synchrony of Ovulation in Red Deer Constrained by Short Northern Summers

Iteroparous mothers often face a trade‐off between further investments in current offspring at the expense of the start of the next reproductive cycle. In the strongly seasonal environments at northern latitudes, large herbivores are typically calving in early summer each year to get a long growth season and to hit peak protein levels of vegetation. Late‐born offspring are more likely to die since they are smaller in autumn. Low female condition in autumn due to prolonged investment in current‐year offspring may lower her ability to ovulate sufficiently early to get a good start for the calves the following spring. On the basis of autopsies of uteri from 10,073 red deer (Cervus elaphus), we show that ovulation was delayed as well as more synchronous with increasing population density. This suggests that ovulation beyond a certain date incurs some fitness costs. Ovulation occurs progressively earlier with increasing age up to around 13 yr of age, after which ovulation again occurs later. Low ovulation rates in young compared with prime‐aged deer were correlated with late ovulation in the fall. Also, yearling groups with a low rate of ovulation (e.g., because of low weight) also ovulated later, and old senescent deer not calving the previous year ovulated less frequently and markedly later than those raising a calf. Our findings suggest, therefore, that mothers unable to ovulate before a certain date fail to do so altogether that year.

[1]  Atle Mysterud,et al.  Temporal variation in the number of car-killed red deer Cervus elaphus in Norway , 2004, Wildlife Biology.

[2]  A. Mysterud,et al.  Review article. Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  O. Hüppop,et al.  North Atlantic Oscillation and timing of spring migration in birds , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  Atle Mysterud,et al.  The role of males in the dynamics of ungulate populations , 2002 .

[5]  A. Mysterud,et al.  Age– and density–dependent reproductive effort in male red deer , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Eric R. Ziegel,et al.  Generalized Linear Models , 2002, Technometrics.

[7]  Atle Mysterud,et al.  Large‐scale habitat variability, delayed density effects and red deer populations in Norway , 2002 .

[8]  A. Mysterud,et al.  Age-related reproductive effort in reindeer (Rangifer tarandus): evidence of senescence , 2002, Oecologia.

[9]  A. Mysterud,et al.  Plant phenology, migration and geographical variation in body weight of a large herbivore: the effect of a variable topography , 2001 .

[10]  B T Grenfell,et al.  Age, sex, density, winter weather, and population crashes in Soay sheep. , 2001, Science.

[11]  A. Mysterud,et al.  Effects of age, sex and density on body weight of Norwegian red deer: evidence of density–dependent senescence , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  Atle Mysterud,et al.  Nonlinear effects of large-scale climatic variability on wild and domestic herbivores , 2001, Nature.

[13]  J. Gaillard,et al.  Temporal Variation in Fitness Components and Population Dynamics of Large Herbivores , 2000 .

[14]  P. Bateson,et al.  The effects of wound site and blood collection method on biochemical measures obtained from wild, free-ranging red deer (Cervus elaphus) shot by rifle. , 2000 .

[15]  A. Sinclair,et al.  WHAT DETERMINES PHENOLOGY AND SYNCHRONY OF UNGULATE BREEDING IN SERENGETI , 2000 .

[16]  Gary L. Dusek,et al.  Evaluating the Accuracy of Ages Obtained by Two Methods for Montana Ungulates , 2000 .

[17]  J. Gaillard,et al.  Body mass and individual fitness in female ungulates: bigger is not always better , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  T. Clutton‐Brock,et al.  On harvesting a structured ungulate population , 2000 .

[19]  M. Festa‐Bianchet,et al.  INDIVIDUAL DIFFERENCES, LONGEVITY, AND REPRODUCTIVE SENESCENCE IN BIGHORN EWES , 1999 .

[20]  Anne Loison,et al.  Consequences of harvesting on age structure, sex ratio and population dynamics of red deer Cervus elaphus in central Norway , 1999, Wildlife Biology.

[21]  Nils Chr. Stenseth,et al.  CLIMATIC VARIABILITY, PLANT PHENOLOGY, AND NORTHERN UNGULATES , 1999 .

[22]  P. E. Komers,et al.  Timing of Estrus in Fallow Deer Is Adjusted to the Age of Available Mates , 1999, The American Naturalist.

[23]  J. Gaillard,et al.  Mass‐ and Density‐Dependent Reproductive Success and Reproductive Costs in a Capital Breeder , 1998, The American Naturalist.

[24]  J. Gaillard,et al.  Population dynamics of large herbivores: variable recruitment with constant adult survival. , 1998, Trends in ecology & evolution.

[25]  N. Stenseth,et al.  Breeding phenology and climate⃛ , 1998, Nature.

[26]  T. Clutton‐Brock,et al.  Density–related changes in sexual selection in red deer , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  Shripad Tuljapurkar,et al.  Structured-Population Models in Marine, Terrestrial, and Freshwater Systems , 1997, Population and Community Biology Series.

[28]  N. Stenseth,et al.  Global climate change and phenotypic variation among red deer cohorts , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  B. Sæther Environmental stochasticity and population dynamics of large herbivores: a search for mechanisms. , 1997, Trends in ecology & evolution.

[30]  B. Ripley,et al.  Modern Applied Statistics with S-Plus. , 1996 .

[31]  T. Clutton‐Brock,et al.  Climate, plant phenology and variation in age of first reproduction in a temperate herbivore , 1996 .

[32]  J. Hurrell Decadal Trends in the North Atlantic Oscillation: Regional Temperatures and Precipitation , 1995, Science.

[33]  M. Festa‐Bianchet,et al.  Life History Consequences of Variation in Age of Primiparity in Bighorn Ewes , 1995 .

[34]  S. Engen,et al.  Retrospective Studies of Red Deer Reproduction Using Regressing Luteal Structures , 1994 .

[35]  F. Messier,et al.  Reproductive Behavior of Male Wood Bison in Relation to Progesterone Level in Females , 1994 .

[36]  J. Gaillard,et al.  SENESCENCE IN NATURAL POPULATIONS OF MAMMALS: A REANALYSIS , 1994, Evolution; international journal of organic evolution.

[37]  J. Hogg,et al.  Sex-biased maternal expenditure in Rocky Mountain bighorn sheep , 1992, Behavioral Ecology and Sociobiology.

[38]  R. Langvatn Analysis of ovaries in studies of reproduction in red deer (Cervus elaphus, L.): Application and limitations , 1992 .

[39]  J. Berger Facilitation of Reproductive Synchrony by Gestation Adjustment in Gregarious Mammals: A New Hypothesis , 1992 .

[40]  Marco Festa-Bianchet,et al.  Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis) , 1989 .

[41]  T. Clutton‐Brock,et al.  Fitness costs of gestation and lactation in wild mammals , 1989, Nature.

[42]  K. McComb Roaring by red deer stags advances the date of oestrus in hinds , 1987, Nature.

[43]  T. Clutton‐Brock,et al.  Interactions Between Population Density and Maternal Characteristics Affecting Fecundity and Juvenile Survival in Red Deer , 1987 .

[44]  F. Guinness,et al.  Synchrony of oestrus and conception in red deer (Cervus elaphus L.) , 1985, Animal Behaviour.

[45]  T. Clutton‐Brock,et al.  The Costs of Reproduction to Red Deer Hinds , 1983 .

[46]  A. Loudon,et al.  Nutrition and lactational control of fertility in red deer , 1983, Nature.

[47]  W. G. Cochran,et al.  Controlling Bias in Observational Studies: A Review. , 1974 .

[48]  F. Guinness,et al.  The reproductive cycle of the female red deer, Cervus elaphus L. , 1971, Journal of reproduction and fertility.

[49]  E. Reimers,et al.  Relationship between Age and Tooth Cementum Layers in Norwegian Reindeer , 1968 .

[50]  A. Mysterud,et al.  The effect of sex ratio and male age structure on reindeer calving , 2003 .

[51]  T. Laaksonen,et al.  Interactive effects of parental age and environmental variation on the breeding performance of Tengmalm's owls , 2002 .

[52]  A. Atkinson Subset Selection in Regression , 1992 .

[53]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[54]  C. Fowler A Review of Density Dependence in Populations of Large Mammals , 1987 .