Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Responses of phenology, synchrony and fecundity of breeding by African ungulates to interannual variation in rainfall

Joseph O. Ogutu A B D , Hans-Peter Piepho B and Holly T. Dublin C
+ Author Affiliations
- Author Affiliations

A International Livestock Research Institute, PO Box 30709, Nairobi 00100, Kenya.

B University of Hohenheim, Institute for Crop Science, Bioinformatics Unit, 70599 Stuttgart, Germany.

C Species Survival Commission (SSC), The World Conservation Union (IUCN), c/o South African National Biodiversity Institute, Centre for Biodiversity Conservation, Private Bag X7, Claremont 7735, Cape Town, Republic of South Africa.

D Corresponding author. Email: jogutu2007@gmail.com

Wildlife Research 40(8) 698-717 https://doi.org/10.1071/WR13117
Submitted: 25 June 2013  Accepted: 14 February 2014   Published: 20 March 2014

Abstract

Context: The timing and synchrony of births are important components of fitness among ungulates living in seasonal environments.

Aims: We investigated the effects of rainfall variation on interannual variation in the timing, synchrony and prolificity of births for six African ungulate species inhabiting an equatorial savanna with bimodal rainfall.

Methods: We analyse how seasonally and aseasonally breeding African savanna ungulates maintain reproductive success despite rainfall constraints, and adjust the phenology, synchrony and fecundity of their breeding to track interannual variation in rainfall. We use data on six ungulate species inhabiting the Masai Mara National Reserve (Mara) of Kenya to test five hypotheses concerning the influences of seasonality in resources, gestation length and the hider–follower strategy on the timing, synchrony and prolificity of calving.

Key results: Births were more synchronised for topi, warthog and zebra than for hartebeest, impala, and giraffe. Births occurred in most months, but tended to peak during the early rains when forage quality peaks for all species. The rainfall component exerting the strongest influence on timing of births varied with species. Gestation length, the hider–follower dichotomy, and hence predation, had apparently weak influences on birth synchrony. In drought years with nutritionally deficient forage, births were delayed, less synchronised and fewer. This portrayed protracted calving seasons, suppression of early conceptions, and delayed onset of births, calf losses, reproductive pauses or failures. However, in rainy years with sufficient forage, births peaked early, or were not delayed, and the synchronicity of calving increased for all species. This suggested early breeding by primiparous females; or higher fertility early in the mating period. The prolificity of calving increased with rainfall for topi and warthog but decreased for the remaining species.

Conclusions: Marked interannual variability in rainfall, plant phenology and forage sufficiency in tropical savannas impose strong constraints on ungulates, favouring flexible timing of births over strictly seasonal reproduction characteristic of temperate latitudes with predictable seasonal resource cues.

Implications: Despite high flexibility in their timing of births, widening rainfall variability expected to result from global warming could lower reproductive success of tropical ungulates by lowering their fecundity and survival prospects of their calves if droughts became more frequent and severe.

Additional keywords: rainfall variability, reproduction.


References

Adams, L. G., and Dale, B. W. (1998). Timing and synchrony of parturition in Alaskan caribou. Journal of Mammalogy 79, 287–294.
Timing and synchrony of parturition in Alaskan caribou.Crossref | GoogleScholarGoogle Scholar |

Ahrestani, F. S., Van Langevelde, F., Heitkönig, I. M. A., and Prins, H. H. T. (2012). Contrasting timing of parturition of chital Axis axis and gaur Bos gaurus in tropical South India – the role of body mass and seasonal forage quality. Oikos 121, 1300–1310.
Contrasting timing of parturition of chital Axis axis and gaur Bos gaurus in tropical South India – the role of body mass and seasonal forage quality.Crossref | GoogleScholarGoogle Scholar |

Aitken, R. J. (1974). Delayed implantation in roe deer (Capreolus capreolus). Journal of Reproduction and Fertility 39, 225–233.
Delayed implantation in roe deer (Capreolus capreolus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c3pvF2rsw%3D%3D&md5=876db29b723925300ba8b36d3db2ab20CAS | 4851283PubMed |

Albon, S. D., and Langvatn, R. (1992). Plant phenology and the benefits of migration in a temperate ungulate. Oikos 65, 502–513.
Plant phenology and the benefits of migration in a temperate ungulate.Crossref | GoogleScholarGoogle Scholar |

Albon, S. D., Mitchell, B., Huby, B. J., and Brown, D. (1986). Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status. Journal of Zoology 209, 447–460.
Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status.Crossref | GoogleScholarGoogle Scholar |

Albon, S. D., Clutton-Brock, T. H., Major, M., and Guinness, F. E. (1987). Early development and population dynamics in red deer. II. Density-independent effects and cohort variation. Journal of Animal Ecology 56, 69–81.
Early development and population dynamics in red deer. II. Density-independent effects and cohort variation.Crossref | GoogleScholarGoogle Scholar |

Andersen, R., Gaillard, J.-M., Linnell, J. D. C., and Duncan, P. (2000). Factors affecting maternal care in an income breeder, the European roe deer. Journal of Animal Ecology 69, 672–682.
Factors affecting maternal care in an income breeder, the European roe deer.Crossref | GoogleScholarGoogle Scholar |

Baker, J. R. (1938). The evolution of breeding seasons. In ‘Evolution’. (Ed. G. R. de Beer.) pp. 161–177. (Clarendon Press: Oxford, UK.)

Beehner, J. C., Onderdonk, D. A., Alberts, S. C., and Altmann, J. (2006). The ecology of conception and pregnancy failure in wild baboons. Behavioral Ecology 17, 741–750.
The ecology of conception and pregnancy failure in wild baboons.Crossref | GoogleScholarGoogle Scholar |

Bercovitch, F. B., Bashaw, M. J., Penny, C. G., and Rieches, R. G. (2004). Maternal investment in captive giraffes. Journal of Mammalogy 85, 428–431.
Maternal investment in captive giraffes.Crossref | GoogleScholarGoogle Scholar |

Berger, J. (1992). Facilitation of reproductive synchrony by gestation adjustment in gregarious mammals: a new hypothesis. Ecology 73, 323–329.
Facilitation of reproductive synchrony by gestation adjustment in gregarious mammals: a new hypothesis.Crossref | GoogleScholarGoogle Scholar |

Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., and White, J. S. S. (2009). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.
Generalized linear mixed models: a practical guide for ecology and evolution.Crossref | GoogleScholarGoogle Scholar |

Bonenfant, C., Gaillard, J.-M., Klein, F., and Hamann, J. L. (2005). Can we use the young: female ratio to infer ungulate population dynamics? An empirical test using red deer Cervus elaphus as a model. Journal of Applied Ecology 42, 361–370.
Can we use the young: female ratio to infer ungulate population dynamics? An empirical test using red deer Cervus elaphus as a model.Crossref | GoogleScholarGoogle Scholar |

Boshe, J. I. (1981). Reproductive ecology of the warthog Pahrcochoerus aethiopicus and its significance for management in the eastern Selous Game Reserve, Tanzania. Biological Conservation 20, 37–44.
Reproductive ecology of the warthog Pahrcochoerus aethiopicus and its significance for management in the eastern Selous Game Reserve, Tanzania.Crossref | GoogleScholarGoogle Scholar |

Boutton, T. W., Tieszen, L. L., and Imbamba, S. K. (1988a). Seasonal changes in the nutrient of East African grassland vegetation. African Journal of Ecology 26, 103–115.
Seasonal changes in the nutrient of East African grassland vegetation.Crossref | GoogleScholarGoogle Scholar |

Boutton, T. W., Tieszen, L. L., and Imbamba, S. K. (1988b). Biomass dynamics of grassland vegetation in Kenya. African Journal of Ecology 26, 89–101.
Biomass dynamics of grassland vegetation in Kenya.Crossref | GoogleScholarGoogle Scholar |

Bowyer, R. T. (1991). Timing of parturition and lactation in southern mule deer. Journal of Mammalogy 72, 138–145.
Timing of parturition and lactation in southern mule deer.Crossref | GoogleScholarGoogle Scholar |

Bradshaw, W. E., and Holzapfel, C. M. (2007). Evolution of animal photoperiodism. Annual Review of Ecology Evolution and Systematics 38, 1–25.
Evolution of animal photoperiodism.Crossref | GoogleScholarGoogle Scholar |

Bro-Jørgensen, J. (2001). Lek-breeding in topi antelopes (Damaliscus lunatus). Ph.D. Thesis, University College London.

Bronson, F. H. (1985). Mammalian reproduction: an ecological perspective. Biology of Reproduction 32, 1–26.
Mammalian reproduction: an ecological perspective.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7itlShsQ%3D%3D&md5=406ce09ae56e38b900176882770d8fcfCAS | 3882162PubMed |

Bronson, F. H. (2009). Climate change and seasonal reproduction in mammals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 3331–3340.
Climate change and seasonal reproduction in mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnpsFamtw%3D%3D&md5=77cdd608401163b4ec4b214c04dafb20CAS | 19833645PubMed |

Bunnell, F. L. (1982). The lambing period of mountain sheep: synthesis, hypotheses, and tests. Canadian Journal of Zoology 60, 1–14.
The lambing period of mountain sheep: synthesis, hypotheses, and tests.Crossref | GoogleScholarGoogle Scholar |

Burthe, S., Butler, A., Searle, K. R., Hall, S. J. G., Thackeray, S. J., and Wanless, S. (2011). Demographic consequences of increased winter births in a large aseasonally breeding mammal (Bos taurus) in response to climate change. Journal of Animal Ecology 80, 1134–1144.
Demographic consequences of increased winter births in a large aseasonally breeding mammal (Bos taurus) in response to climate change.Crossref | GoogleScholarGoogle Scholar | 21668894PubMed |

Clements, M. N., Clutton-Brock, T. H., Albon, D. A., Pemberton, J. M., and Kruuk, L. E. B. (2011). Gestation length variation in a wild ungulate. Functional Ecology 25, 691–703.
Gestation length variation in a wild ungulate.Crossref | GoogleScholarGoogle Scholar |

Clutton-Brock, T. H., Guinness, F. E., and Albon, S. D. (1982). ‘Red Deer: Behaviour and Ecology of Two Sexes.’ (University of Chicago Press: Chicago, IL.)

Clutton-Brock, T. H., Major, M., Albon, S. D., and Guinness, F. E. (1987). Early development and population dynamics in red deer. I. Density-dependent effects on juvenile survival. Journal of Animal Ecology 56, 53–67.
Early development and population dynamics in red deer. I. Density-dependent effects on juvenile survival.Crossref | GoogleScholarGoogle Scholar |

Clutton-Brock, T. H., Albon, S. D., and Guinness, F. E. (1989). Fitness costs of gestation and lactation in wild mammals. Nature 337, 260–262.
Fitness costs of gestation and lactation in wild mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FpslaksA%3D%3D&md5=dfe01360424ce00118a25b1e1c0eeab7CAS | 2911365PubMed |

Cook, J. G., Quinlan, L. J., Irwin, L. L., Bryant, L. D., Riggs, R. A., and Thomas, J. W. (1996). Nutrition-growth relations of elk calves during late summer and fall. The Journal of Wildlife Management 60, 528–541.
Nutrition-growth relations of elk calves during late summer and fall.Crossref | GoogleScholarGoogle Scholar |

Cook, R. C., Murray, D. L., Cook, J. G., Zager, P., and Monfort, S. L. (2001). Nutritional influences on breeding dynamics in elk. Canadian Journal of Zoology 79, 845–853.
Nutritional influences on breeding dynamics in elk.Crossref | GoogleScholarGoogle Scholar |

Cook, J. G., Johnson, B. K., Cook, R. C., Riggs, R. A., Delcurto, T., Bryant, L. D., and Irwin, L. L. (2004). Effects of summer–autumn nutrition and parturition date on reproduction and survival of elk. Wildlife Monographs 155, 1–61.

Côté, S.D., and Festa-Bianchet, M. (2001). Birthdate, mass and survival in mountain kids: effects of maternal characteristic and forage quality. Oecologia 127, 230–238.
Birthdate, mass and survival in mountain kids: effects of maternal characteristic and forage quality.Crossref | GoogleScholarGoogle Scholar | 24577654PubMed |

Cumming, D. H. (1975). ‘A Field Study of the Ecology and Behaviour of Warthog. Vol. 7.’ (Trustees of the National Museums and Monuments of Rhodesia: Salisbury, Rhodesia.)

Deshmukh, I. K. (1984). A common relationship between precipitation and grassland peak biomass for East and southern Africa. African Journal of Ecology 22, 181–186.
A common relationship between precipitation and grassland peak biomass for East and southern Africa.Crossref | GoogleScholarGoogle Scholar |

du Plessis, S. S. (1972). ‘Ecology of Blesbok with Special Reference to Productivity.’ Wildlife Monographs. No. 30. (The Wildlife Society: Washington, DC.)

Dublin, H. T. (1994). Kenya: the 1993 record drought. In ‘Gnusletter 13, Nos 1 and 2’. (Ed. R. D. Estes) pp. 14–15. (Antelope Specialist Group, The World Conservation Union: Peterborough, NH.)

Duncan, P. (1975). Topi and their food supply. Ph.D. Thesis, University of Nairobi, Kenya.

Dunham, K. M., and Murray, M. G. (1982). The fat reserves of impala, Aepyceros melampus. African Journal of Ecology 20, 81–87.
The fat reserves of impala, Aepyceros melampus.Crossref | GoogleScholarGoogle Scholar |

Estes, R. D. (1976). The significance of breeding synchrony in the wildebeest. East African Wildlife Journal 14, 135–152.
The significance of breeding synchrony in the wildebeest.Crossref | GoogleScholarGoogle Scholar |

Estes, R. D. (1991). ‘The Behavior Guide to African Mammals.’ (University of California Press: Los Angeles, CA.)

Estes, R. D., Atwood, J. L., and Estes, A. B. (2006). Downward trends in Ngorongoro Crater ungulate populations 1986–2005: conservation concerns and the need for ecological research. Biological Conservation 131, 106–120.
Downward trends in Ngorongoro Crater ungulate populations 1986–2005: conservation concerns and the need for ecological research.Crossref | GoogleScholarGoogle Scholar |

Fairall, N. (1968). The reproductive seasons of some mammals in the Kruger National Park. Zoologica Africana 3, 180–210.

Fairall, N. (1983). Production parameters of the impala, Aepyceros melampus. South African Journal of Animal Science 13, 176–179.

Festa-Bianchet, M., Jorgenson, J. T., and Reale, D. (2000). Early development, adult mass, and reproductive success in bighorn sheep. Behavioral Ecology 11, 633–639.
Early development, adult mass, and reproductive success in bighorn sheep.Crossref | GoogleScholarGoogle Scholar |

Foster, J. B., and Dagg, A. I. (1972). Notes on the ecology of the giraffe. East African Wildlife Journal 10, 1–16.
Notes on the ecology of the giraffe.Crossref | GoogleScholarGoogle Scholar |

Gaillard, J. M., Delorme, D., and Julien, J. M. (1993a). Effects of cohort, sex and birth date on body development of roe deer (Capreolus capreolus) fawns. Oecologia 94, 57–61.
Effects of cohort, sex and birth date on body development of roe deer (Capreolus capreolus) fawns.Crossref | GoogleScholarGoogle Scholar |

Gaillard, J. M., Delorme, D., Julien, J. M., and Tatin, D. (1993b). Timing and synchrony of births in roe deer. Journal of Mammalogy 74, 738–744.
Timing and synchrony of births in roe deer.Crossref | GoogleScholarGoogle Scholar |

Georgiadis, N., and McNaughton, S. J. (1990). Elemental and fibre contents of savanna grasses: variation with grazing, soil type, season and species. Journal of Applied Ecology 27, 623–634.
Elemental and fibre contents of savanna grasses: variation with grazing, soil type, season and species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhs1akt7s%3D&md5=b537e255e154a14f53b71a5bf4c9f638CAS |

Georgiadis, N., Hack, M., and Turpin, K. (2003). The influence of rainfall on zebra population dynamics: implications for management. Journal of Applied Ecology 40, 125–136.
The influence of rainfall on zebra population dynamics: implications for management.Crossref | GoogleScholarGoogle Scholar |

Gogan, P. J. P., Podruzny, K. M., Olexa, E. M., Pac, H. I., and Frey, K. L. (2005). Yellowstone bison fetal development and phenology of parturition. The Journal of Wildlife Management 69, 1716–1730.
Yellowstone bison fetal development and phenology of parturition.Crossref | GoogleScholarGoogle Scholar |

Gosling, L. M. (1969). Parturition and related behavior in Coke’s hartebeest, Alcelaphus buselaphus cokei Günther. Journal of Reproduction and Fertility. Supplement 6, 265–286.

Green, W. C. H., and Rothstein, A. (1993). Persistent influences of birth date on dominance, growth and reproductive success in bison. Journal of Zoology 230, 177–186.
Persistent influences of birth date on dominance, growth and reproductive success in bison.Crossref | GoogleScholarGoogle Scholar |

Grimsdell, J. J. R. (1973). Reproduction in the African buffalo (Syncerus caffer) in western Uganda. Journal of Reproduction and Fertility. Supplement 19, 303–318.
| 1:STN:280:DyaE2c7ivVWntg%3D%3D&md5=f0365b1544cc9840b7bcd13be48c0719CAS |

Guinness, F. E., Clutton-Brock, T. H., and Albon, S. D. (1978). Factors affecting calf mortality in red deer (Cervus elaphus). Journal of Animal Ecology 47, 817–832.
Factors affecting calf mortality in red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar |

Gunn, R. G., and Doney, J. M. (1975). The interaction of nutrition and physical condition at mating on ovulation rate and early embryo mortality in Scottish blackface ewes. Journal of Agricultural Science (Cambridge) 85, 465–470.
The interaction of nutrition and physical condition at mating on ovulation rate and early embryo mortality in Scottish blackface ewes.Crossref | GoogleScholarGoogle Scholar |

Hall-Martin, A. J., Skinner, J. D., and Van Dyk, J. M. (1975). Reproduction in the giraffe in relation to some environmental factors. East African Wildlife Journal 13, 237–248.
Reproduction in the giraffe in relation to some environmental factors.Crossref | GoogleScholarGoogle Scholar |

Hass, C. C. (1997). Seasonality of births in bighorn sheep. Journal of Mammalogy 78, 1251–1260.
Seasonality of births in bighorn sheep.Crossref | GoogleScholarGoogle Scholar |

Jönsson, K. I. (1997). Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78, 57–66.
Capital and income breeding as alternative tactics of resource use in reproduction.Crossref | GoogleScholarGoogle Scholar |

Jorgenson, J. T., Festa-Bianchet, M., Lucherini, M., and Wishart, W. D. (1993). Effects of body size, population density, and maternal characteristics on age at first reproduction in bighorn ewes. Canadian Journal of Zoology 71, 2509–2517.
Effects of body size, population density, and maternal characteristics on age at first reproduction in bighorn ewes.Crossref | GoogleScholarGoogle Scholar |

Keech, M. A., Bowyer, R. T., Ver Hoef, J. M., Boertje, R. D., Dale, B. W., and Stephenson, R. (2000). Life-history consequences of maternal condition in Alaskan moose. The Journal of Wildlife Management 64, 450–462.
Life-history consequences of maternal condition in Alaskan moose.Crossref | GoogleScholarGoogle Scholar |

Kieltie, R. A. (1988). Gestation as a constraint on the evolution of seasonal breeding in mammals. In ‘Evolution of Life Histories of Mammals. Theory and Pattern’. (Ed. M. S. Boyce.) pp. 257–289. (Yale University Press: New Haven, CT.)

Kim, Y., Choi, Y.-K., and Emery, S. (2013). A logistic regression with multiple random effects: a simulation study of estimation methods and statistical packages. The American Statistician 67, 171–182.
A logistic regression with multiple random effects: a simulation study of estimation methods and statistical packages.Crossref | GoogleScholarGoogle Scholar |

Kingdon, A. (1989). ‘East African Mammals: an Atlas of Evolution in Africa. Vol. III. Part D (Bovids).’ (University of Chicago Press: Chicago, IL.)

Kingdon, J. (1997). ‘The Kingdon Field Guide to African Mammals.’ (Academic Press: London.)

Langman, V. A. (1977). Cow-calf relationships in giraffe (Giraffa camelopardalis giraffa). Zeitschrift für Tierpsychologie 43, 264–286.

Langvatn, R., Mysterud, A., Stenseth, N. C., and Yoccoz, N. G. (2004). Timing and synchrony of ovulation in red deer constrained by short northern summers. American Naturalist 163, 763–772.
Timing and synchrony of ovulation in red deer constrained by short northern summers.Crossref | GoogleScholarGoogle Scholar | 15122493PubMed |

Leuthold, W., and Leuthold, B. M. (1975). Temporal patterns of reproduction in ungulates of Tsavo East National Park, Kenya. East African Wildlife Journal 13, 159–169.
Temporal patterns of reproduction in ungulates of Tsavo East National Park, Kenya.Crossref | GoogleScholarGoogle Scholar |

Loudon, A. S. I., Darroch, A. D., and Milne, J. A. (1984). The lactation performance of red deer on hill and improved species pastures. Journal of Agricultural Science 102, 149–158.
The lactation performance of red deer on hill and improved species pastures.Crossref | GoogleScholarGoogle Scholar |

Moe, S. R., Rutina, L. P., and du Toit, J. T. (2007). Trade-off between resource seasonality and predation risk explains reproductive chronology in impala. Journal of Zoology 273, 237–243.
Trade-off between resource seasonality and predation risk explains reproductive chronology in impala.Crossref | GoogleScholarGoogle Scholar |

Moss, C. J. (2001). The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. Journal of Zoology 255, 145–156.
The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya.Crossref | GoogleScholarGoogle Scholar |

Moyes, K., Nussey, D. H., Clements, M. N., Guinness, F. E., Morris, A., Morris, S., Pemberton, J. M., Kruuk, L. E. B., and Clutton-Brock, T. H. (2011). Advancing breeding phenology in response to environmental change in a wild red deer population. Global Change Biology 17, 2455–2469.
Advancing breeding phenology in response to environmental change in a wild red deer population.Crossref | GoogleScholarGoogle Scholar |

Murray, M. G. (1982). The rut of impala: aspects of seasonal mating under tropical conditions. Zetischrift für Tierpsychology 59, 319–337.
The rut of impala: aspects of seasonal mating under tropical conditions.Crossref | GoogleScholarGoogle Scholar |

Nefdt, R. J. C. (1996). Reproductive seasonality in Kafue lechwe antelope. Journal of Zoology 239, 155–166.
Reproductive seasonality in Kafue lechwe antelope.Crossref | GoogleScholarGoogle Scholar |

Novellie, P. (1986). Relationships between rainfall, population density and the size of the bontebok lamb crop in the Bontebok National Park. South African Journal of Wildlife Research 16, 39–46.

Oftedal, O. T. (1985). Pregnancy and lactation. In ‘Bioenergetics of Wild Herbivores’. (Ed. R. J. Hudson and R. G. White.) pp. 215–238. (CRC Press: Boca Raton, FL.)

Ogutu, J. O., Bhola, N., Piepho, H.-P., and Reid, R. (2006). Efficiency of strip- and line-transect surveys of African savanna mammals. Journal of Zoology 269, 149–160.

Ogutu, J. O., Piepho, H.-P., Dublin, H. T., Bhola, N., and Reid, R. S. (2008a). El Niño–Southern Oscillation, rainfall, temperature and normalised difference vegetation index fluctuations in the Mara–Serengeti ecosystem. African Journal of Ecology 46, 132–143.
El Niño–Southern Oscillation, rainfall, temperature and normalised difference vegetation index fluctuations in the Mara–Serengeti ecosystem.Crossref | GoogleScholarGoogle Scholar |

Ogutu, J. O., Piepho, H.-P., Dublin, H. T., Bhola, N., and Reid, R. S. (2008b). Rainfall influences on ungulate population abundance in the Mara–Serengeti ecosystem. Journal of Animal Ecology 77, 814–829.
Rainfall influences on ungulate population abundance in the Mara–Serengeti ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvgsFynug%3D%3D&md5=c46969a9525582191775d3353a658e4dCAS | 18422558PubMed |

Ogutu, J. O., Piepho, H.-P., Dublin, H. T., Bhola, N., and Reid, R. S. (2009). Dynamics of Mara–Serengeti ungulates in relation to land use changes. Journal of Zoology 278, 1–14.
Dynamics of Mara–Serengeti ungulates in relation to land use changes.Crossref | GoogleScholarGoogle Scholar |

Ogutu, J. O., Piepho, H.-P., Dublin, H. T., Bhola, N., and Reid, R. S. (2010). Rainfall extremes explain interannual shifts in timing and synchrony of calving in topi and warthog. Population Ecology 52, 89–102.
Rainfall extremes explain interannual shifts in timing and synchrony of calving in topi and warthog.Crossref | GoogleScholarGoogle Scholar |

Ogutu, J. O., Piepho, H.-P., Dublin, H. T., Bhola, N., and Reid, R. S. (2011). Dynamics of births and juvenile recruitment in Mara–Serengeti ungulates in relation to climatic and land use changes. Population Ecology 53, 195–213.
Dynamics of births and juvenile recruitment in Mara–Serengeti ungulates in relation to climatic and land use changes.Crossref | GoogleScholarGoogle Scholar |

Owen-Smith, R. N. (1988). ‘Mega Herbivores: the Influence of Very Large Body Size on Ecology.’ (Cambridge University Press: Cambridge, UK.)

Owen-Smith, N. (2002). ‘Adaptive Herbivore Ecology. From Resources to Populations in Variable Environments.’ (Cambridge University Press: Cambridge, UK.)

Owen-Smith, N. (2008). The comparative population dynamics of browsing and grazing ungulates. In ‘The Ecology of Grazing and Browsing Ungulates’. (Eds I. J. Gordon and H. H. T. Prins.) pp. 149–177. (Spinger Verlag: Berlin.)

Owen-Smith, N., and Ogutu, J. O. (2013). Controls over reproductive phenology among ungulates: allometry and tropical–temperate contrasts. Ecography 36, 256–263.
Controls over reproductive phenology among ungulates: allometry and tropical–temperate contrasts.Crossref | GoogleScholarGoogle Scholar |

Parker, K. L., Barboza, P. S., and Gillingham, M. P. (2009). Nutrition integrates environmental responses of ungulates. Functional Ecology 23, 57–69.
Nutrition integrates environmental responses of ungulates.Crossref | GoogleScholarGoogle Scholar |

Penzhorn, B. I. (1985). Reproductive characteristics of a free-ranging population of Cape Mountain zebra (Equus zebra zebra). Journal of Reproduction and Fertility 73, 51–57.
Reproductive characteristics of a free-ranging population of Cape Mountain zebra (Equus zebra zebra).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7gslyhtw%3D%3D&md5=f8ad53ef926f680b2d8a75c5da4ecff8CAS |

Percival, A. B. (1928). ‘A Game Ranger on Safari.’ (Nisbet and Co: London.)

Piepho, H. P., and Ogutu, J. O. (2007). Simple state space models in a mixed model framework. The American Statistician 61, 224–232.
Simple state space models in a mixed model framework.Crossref | GoogleScholarGoogle Scholar |

Post, E. (2003). Timing of reproduction in large mammals. In ‘Phenology: an Integrative Environemental Science’. (Ed. M. D. Schwartz.) pp. 437–449. (Kluwer Academic Publishers: Dordrecht, The Netherlands.)

Post, E., and Forchhammer, M. C. (2008). Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Transactions of the Royal Society Series B 363, 2369–2375.

Post, E., and Stenseth, N. C. (1999). Climatic variability, plant phenology, and northern ungulates. Ecology 80, 1322–1339.
Climatic variability, plant phenology, and northern ungulates.Crossref | GoogleScholarGoogle Scholar |

Post, E., Bøving, P. S., Perdersen, C., and MacArthur, M. A. (2003). Synchrony between caribou calving and plant phenology in depredated and non-depredated populations. Canadian Journal of Zoology 81, 1709–1714.
Synchrony between caribou calving and plant phenology in depredated and non-depredated populations.Crossref | GoogleScholarGoogle Scholar |

Post, E., Pedersen, C., Wilmers, C. C., and Forchhammer, M. C. (2008). Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proceedings of the Royal Society. Series B 275, 2005–2013.
Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores.Crossref | GoogleScholarGoogle Scholar |

Pratt, D. M., and Anderson, V. H. (1982). Population, distribution, and behaviour of giraffe in the Arusha National Park. Tanzania Journal of Natural History 16, 481–489.
Population, distribution, and behaviour of giraffe in the Arusha National Park.Crossref | GoogleScholarGoogle Scholar |

Prins, H. H. T. (1988). Plant phenology patterns in Lake Manyara National Park, Tanzania. Journal of Biogeography 15, 465–480.
Plant phenology patterns in Lake Manyara National Park, Tanzania.Crossref | GoogleScholarGoogle Scholar |

Prins, H. H. T. (1996). ‘Ecology and Behaviour of the African Buffalo: Social Inequality and Decision Making.’ (Chapman and Hall: New York.)

Prins, H. H. T., and Beekman, J. H. (1989). A balanced diet as a goal for grazing: the food of the Manyara buffalo. African Journal of Ecology 27, 241–259.
A balanced diet as a goal for grazing: the food of the Manyara buffalo.Crossref | GoogleScholarGoogle Scholar |

Rutberg, A. T. (1987). Adaptive hypotheses of birth synchrony in ruminants: an interspecific test. American Naturalist 130, 692–710.
Adaptive hypotheses of birth synchrony in ruminants: an interspecific test.Crossref | GoogleScholarGoogle Scholar |

Rutherford, M. C. (1980). Annual plant production–precipitation relations in arid and semi-arid regions. South African Journal of Science 76, 53–56.

Ryan, S. J., Knechtel, C. V., and Getz, W. M. (2007). Ecological cues, gestation length, and birth timing in African buffalo (Syncerus caffer). Behavioral Ecology 18, 635–644.
Ecological cues, gestation length, and birth timing in African buffalo (Syncerus caffer).Crossref | GoogleScholarGoogle Scholar |

Sadleir, R. M. F. S. (1969). ‘The Ecology of Reproduction in Wild and Domestic Animals.’ (Methuen and Co.: London.)

SAS Institute (2013). ‘SAS System for Windows. Version 9.3.’ (SAS Institute: Cary, NC.)

Sidney, O. J. (1965). The past and present distribution of some African ungulates. Transactions of the Zoological Society of London 30, 1–397.

Simon, N. (1962). ‘Between the Sunlight and the Thunder: The Wild Life of Kenya.’ (Collins: London.)

Sinclair, A. R. E., and Duncan, P. (1972). Indices of condition in tropical ruminants. East African Journal of Ecology 10, 143–149.
Indices of condition in tropical ruminants.Crossref | GoogleScholarGoogle Scholar |

Sinclair, A. R. E., Mduma, S. A. R., and Arcese, P. (2000). What determines phenology and synchrony of ungulate breeding in Serengeti? Ecology 81, 2100–2111.
What determines phenology and synchrony of ungulate breeding in Serengeti?Crossref | GoogleScholarGoogle Scholar |

Skinner, J. D., and Chimimba, C. T. (2005). ‘The Mammals of the Southern African Subregion.’ (Cambridge University Press: Cambridge, UK.)

Skinner, J. D., Moss, D. G., and Skinner, D. C. (2002). Inherent seasonality in the breeding seasons of African mammals: evidence from captive breeding. Transactions of the Royal Society of South Africa 57, 25–34.
Inherent seasonality in the breeding seasons of African mammals: evidence from captive breeding.Crossref | GoogleScholarGoogle Scholar |

Sommers, M. J., and Penzhorn, B. L. (1992). Reproduction in a reintroduced warthog population in the eastern Cape Province. South African Journal of Wildlife Research 22, 57–60.

Spinage, C. A. (1973). The role of photoperiodism in the seasonal breeding of tropical African ungulates. Mammal Review 3, 71–83.
The role of photoperiodism in the seasonal breeding of tropical African ungulates.Crossref | GoogleScholarGoogle Scholar |

Stanley-Price, M. R. (1974). The feeding ecology of Coke’s hartebeest, Alcelaphus buselaphus cokei Günther in Kenya. D.Phil. Thesis, University of Oxford, UK.

Stephens, P. A., Boyd, I. L., McNamara, J. M., and Houston, A. I. (2009). Capital breeding and income breeding: their meaning, measurement and worth. Ecolgy 90, 2057–2067.
Capital breeding and income breeding: their meaning, measurement and worth.Crossref | GoogleScholarGoogle Scholar |

Talbot, L. M., and Talbot, M. H. (1963). ‘The Wildebeest in Western Maasialand, East Africa.’ Wildlife Monographs No. 12. (The Wildlife Society: Washington, DC.)

Testa, J. W. (2002). Does predation on neonates inherently select for earlier births? Journal of Mammalogy 83, 699–706.
Does predation on neonates inherently select for earlier births?Crossref | GoogleScholarGoogle Scholar |

Thomas, D. C. (1982). The relationship between fertility and fat reserve in Peary caribou. Canadian Journal of Zoology 60, 597–602.
The relationship between fertility and fat reserve in Peary caribou.Crossref | GoogleScholarGoogle Scholar |

Verme, L. J. (1965). Reproduction studies on penned whitetailed deer. The Journal of Wildlife Management 29, 74–79.
Reproduction studies on penned whitetailed deer.Crossref | GoogleScholarGoogle Scholar |

Walker, B. H., Emslie, R. H., Owen-Smith, R. N., and Scholes, R. J. (1987). To cull or not to cull: lessons from a southern African drought. Journal of Applied Ecology 24, 381–401.
To cull or not to cull: lessons from a southern African drought.Crossref | GoogleScholarGoogle Scholar |

Western, D. (1979). Size, life history and ecology in mammals. African Journal of Ecology 17, 185–204.
Size, life history and ecology in mammals.Crossref | GoogleScholarGoogle Scholar |

Wittemyer, G., Rasmussen, H. B., and Douglas-Hamilton, I. (2007a). Breeding phenology in relation to NDVI variability in free-ranging African elephant. Ecography 30, 42–50.
Breeding phenology in relation to NDVI variability in free-ranging African elephant.Crossref | GoogleScholarGoogle Scholar |

Wittemyer, G., Ganswindt, A., and Hodges, K. (2007b). The impact of ecological variability on the reproductive endocrinology of wild female African elephants. Hormones and Behavior 51, 346–354.
The impact of ecological variability on the reproductive endocrinology of wild female African elephants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXis1Oktr4%3D&md5=0d938d7e3124632bbdd90e051a09bb19CAS | 17320085PubMed |

Zerbe, P., Marcus, C., Codron, D., Lackey, L. B., Rensch, E., Streich, J. W., Hatt, J.-M., and Müller, D. W. H. (2012). Reproductive seasonality in captive wild ruminants: implications for biogeographical, photoperiodic control, and life history. Biological Reviews of the Cambridge Philosophical Society 87, 965–990.
Reproductive seasonality in captive wild ruminants: implications for biogeographical, photoperiodic control, and life history.Crossref | GoogleScholarGoogle Scholar | 22780447PubMed |