Reproductive seasonality in African ungulates in relation to rainfall
Joseph O. Ogutu A B D , Hans-Peter Piepho A and Holly T. Dublin CA University of Hohenheim, Institute for Crop Science-340, Fruwirthstrasse 23, 70599 Stuttgart, Germany.
B International Livestock Research Institute, PO Box 30709, Nairobi, 00100, Kenya.
C The World Conservation Union (IUCN), c/o IUCN ESARO, Wasa Conservation Centre, PO Box 68200, Nairobi 00200, Kenya.
D Corresponding author. Email: jogutu2007@gmail.com
Wildlife Research 41(4) 323-342 https://doi.org/10.1071/WR13211
Submitted: 8 December 2013 Accepted: 12 September 2014 Published: 18 December 2014
Journal Compilation © CSIRO Publishing 2014 Open Access CC BY-NC-ND
Abstract
Context: Reproductive seasonality in ungulates has important fitness consequences but its relationship to resource seasonality is not yet fully understood, especially for ungulates inhabiting equatorial environments.
Aims: We test hypotheses concerning synchronisation of conception or parturition peaks among African ungulates with seasonal peaks in forage quality and quantity, indexed by rainfall.
Methods: We relate monthly apparent fecundity and juvenile recruitment rates to monthly rainfall for six ungulate species inhabiting the Masai Mara National Reserve (Mara) of Kenya, using cross-correlation analysis and distributed lag non-linear models. We compare the phenology and synchrony of breeding among the Mara ungulates with those for other parts of equatorial East Africa, with bimodal rainfall and less seasonal forage variation, and for subtropical southern Africa, with unimodal rainfall distribution and greater seasonal forage variation.
Key results: Births were more synchronised for topi, warthog and zebra than for hartebeest, impala and giraffe in the Mara, and for impala and hartebeest in southern than in eastern Africa. This pattern is likely to reflect regional differences in climate and plant phenology, hider–follower dichotomy and grazing versus browsing. All six species except the browsing giraffe apparently time the conception to occur in one wet season and births to occur just before the onset or during the next wet season, so as to maximise high-quality forage intake during conception and parturition. Fecundity and recruitment rates among the African ungulates peak at intermediate levels of rainfall and are reduced at low or excessive levels of rainfall. Fecundity rate is most strongly positively correlated with rainfall pre-conception, during conception and during early gestation, followed by rainfall at about the time of parturition for all the grazers. For giraffe, fecundity rate is most strongly correlated with rainfall during the gestation period.
Conclusions: Rainfall seasonality strongly influences reproductive seasonality and juvenile recruitment among African ungulates. The interaction of the rainfall influence with life-history traits and other factors leads to wide interspecific and regional variation.
Implications: Global climate change, especially widening annual rainfall variation expected to result from global warming, could reduce the predictability of the timing of peak forage availability and quality based on meteorological cues, the length of time with adequate nutrition or both, and hence reduce reproductive success among tropical ungulates.
Additional keywords: cross-correlations, distributed lag non-linear models, juvenile recruitment, Mara–Serengeti ecosystem.
References
Anderson, J. L. (1979). Reproductive seasonality of the nyala Tragelaphus angasi: the interaction of light, vegetation phenology, feeding style and reproductive physiology. Mammal Review 9, 33–46.| Reproductive seasonality of the nyala Tragelaphus angasi: the interaction of light, vegetation phenology, feeding style and reproductive physiology.Crossref | GoogleScholarGoogle Scholar |
Ansell, W. F. H. (1960). The breeding of some larger mammals in northern Rhodesia. Proceedings of the Zoological Society of London 134, 251–274.
| The breeding of some larger mammals in northern Rhodesia.Crossref | GoogleScholarGoogle Scholar |
Ansell, W. F. H. (1963). Additional breeding data on northern Rhodesian mammals. Puku 1, 9–19.
Bercovitch, F. B., and Berry, P. S. M. (2010). Reproductive life history of Thonicroft’s giraffe in Zambia. African Journal of Ecology 48, 535–538.
| Reproductive life history of Thonicroft’s giraffe in Zambia.Crossref | GoogleScholarGoogle Scholar |
Boutton, T. W., Tieszen, L. L., and Imbamba, S. K. (1988a). Biomass dynamics of grassland vegetation in Kenya. African Journal of Ecology 26, 89–101.
| Biomass dynamics of grassland vegetation in Kenya.Crossref | GoogleScholarGoogle Scholar |
Boutton, T. W., Tieszen, L. L., and Imbamba, S. K. (1988b). 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 |
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 |
Bowyer, R. T., Kie, J. G., and Van Ballenberghe, V. (1998). Habitat selection by neonatal black-tailed deer: climate, forage, or risk of predation? Journal of Mammalogy 79, 415–425.
| Habitat selection by neonatal black-tailed deer: climate, forage, or risk of predation?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). PhD Thesis. University College, London.
Brown, C. E. (1936). Rearing wild animals in captivity and gestation periods. Journal of Mammalogy 17, 10–13.
| Rearing wild animals in captivity and gestation periods.Crossref | GoogleScholarGoogle Scholar |
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. A., 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 |
Carmichael, I. H., Patterson, L., Dräger, N., and Breton, D. A. (1977). Studies on reproduction in the African buffalo (Syncerus caffer) in Botswana. South African Journal of Wildlife Research 7, 45–52.
Chardonnet, P., and Crosmary, W. (2013). Pigs, hippopotamuses, chevrotain, giraffes, deer and bovids. In ‘Mammals of Africa’. (Eds J. Kingdon and M. Hoffmann) pp. 548–556. (Bloomsbury: Londres.).
Child, G. (1968). An ecological survey of north-eastern Botswana. UNDP/FAO Project no. TA 2563. Report to the Government of Botswana. FAO Rome..
Child, G., and Wilson, V. J. (1964). Observations on ecology and behaviour of roan and sable in three tsetse control areas. Arnoldia Rhodesia 16, 1–8.
Clough, G. (1969). Some preliminary observations on reproduction in the warthog, Pharcochoerus aethiopicus Pallas. Journal of Reproduction and Fertility 6, 323–337.
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.)
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.)
Dauphiné, T. C. J., and McClure, R. L. (1974). Synchronous mating in Canadian barren-ground caribou. The Journal of Wildlife Management 38, 54–66.
| Synchronous mating in Canadian barren-ground caribou.Crossref | GoogleScholarGoogle Scholar |
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. pp. 69. (The Wildlife Society: Washington, DC.)
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., and Estes, R. K. (1974). The biology and conservation of the giant sable antelope (Hippotragus niger variani Thomas, 1916). Proceedings. Academy of Natural Sciences of Philadelphia 126, 73–104.
Fairall, N. (1968). The reproductive seasons of some mammals in the Kruger National Park. Zoologica Africana 3, 180–210.
Fairall, N. (1972). Behavioural aspects of the reproductive physiology of the impala, Aepyceros melampus (Litch.). Zoologica Africana 7, 167–174.
Festa-Bianchet, M., Gaillard, J.-M., and Jorgenson, J. T. (1998). Mass and density-dependent reproductive success and reproductive costs in a capital breeder. American Naturalist 152, 367–379.
| Mass and density-dependent reproductive success and reproductive costs in a capital breeder.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FpvFemsg%3D%3D&md5=e3a6028f89ece23e2286085d3443f797CAS | 18811445PubMed |
Field, C. R., and Blankenship, L. H. (1973). Nutrition and reproduction of Grant’s and Thomson’s gazelles, Coke’s hartebeest and giraffe in Kenya. Journal of Reproduction and Fertility 19, 287–301.
| 1:STN:280:DyaE2c7ivVWnsQ%3D%3D&md5=002ff2ca2142a91db1c33cf6085730ecCAS | 4522381PubMed |
Fryxell, J. M. (1987). Seasonal reproduction of white-eared kob in Boma National Park, Sudan. African Journal of Ecology 25, 117–124.
| Seasonal reproduction of white-eared kob in Boma National Park, Sudan.Crossref | GoogleScholarGoogle Scholar |
Gaillard, J.-M., Delorme, D., Julien, J.-M., and Tatin, D. (1993). 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 |
Garel, M., Solberg, E. J., Sæther, B.-E., Grøtan, V., Tufto, J., and Heim, M. (2009). Age, size, and spatiotemporal variation in ovulation patterns of a seasonal breeder, the Norwegian moose (Alces alces). American Naturalist 173, 89–104.
| Age, size, and spatiotemporal variation in ovulation patterns of a seasonal breeder, the Norwegian moose (Alces alces).Crossref | GoogleScholarGoogle Scholar | 19072136PubMed |
Gasparrini, A. (2011). Distributed lag linear and non-linear models in R: the package dlnm. Journal of Statistical Software 43, 1–20.
| 22003319PubMed |
Gasparrini, A., and Armstrong, B. (2013). Reducing and meta-analyzing estimates from distributed lag non-linear models. BMC Medical Research Methodology 13, 1.
| Reducing and meta-analyzing estimates from distributed lag non-linear models.Crossref | GoogleScholarGoogle Scholar | 23297754PubMed |
Gasparrini, A., Armstrong, B., and Kenward, M. G. (2010). Distributed lag non-linear models. Statistics in Medicine 29, 2224–2234.
| Distributed lag non-linear models.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjpt1ChtQ%3D%3D&md5=1a70eada71948c29a61d8f1661026c56CAS | 20812303PubMed |
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 |
Grimsdell, J. J. R. (1973). Reproduction in the African buffalo (Syncerus caffer) in western Uganda. Journal of Reproduction and Fertility 19, 303–318.
| 1:STN:280:DyaE2c7ivVWntg%3D%3D&md5=f0365b1544cc9840b7bcd13be48c0719CAS |
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 |
Ims, R. A. (1990). On the adaptive value of reproductive synchrony as a predator-swamping strategy. American Naturalist 136, 485–498.
| On the adaptive value of reproductive synchrony as a predator-swamping strategy.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 |
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 |
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 |
Lewis, R. J., and Kappeler, P. M. (2005). Are Kirindy Sifaka capital or income breeders? It depends. American Journal of Primatology 67, 365–369.
| Are Kirindy Sifaka capital or income breeders? It depends.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mnhs1Srtg%3D%3D&md5=ffe13b9640109b33c7e43bf1a0e2dd9fCAS | 16287106PubMed |
Linnell, J. D. C., and Andersen, R. (1998). Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus. Journal of Zoology 244, 497–504.
| Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus.Crossref | GoogleScholarGoogle Scholar |
Mason, D. R. (1986). Reproduction in the male warthog Pharcocoerus aethiopicus from Zululand, South Africa. South African Journal of Zoology 21, 39–47.
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 |
Morrow, C. J., Wildt, D. E., and Monfort, S. L. (1999). Reproductive seasonality in the female scimitar-horned oryx (Oryx dammah). Animal Conservation 2, 261–268.
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 the impala: aspects of seasonal mating under tropical conditions. Zeitschrift für Tierpsychologie 59, 319–337.
| The rut of the impala: aspects of seasonal mating under tropical conditions.Crossref | GoogleScholarGoogle Scholar |
Ndibalema, V. G. (2009). A comparison of sex ratio, birth periods and calf survival among Serengeti wildebeest sub-populations, Tanzania. African Journal of Ecology 47, 574–582.
| A comparison of sex ratio, birth periods and calf survival among Serengeti wildebeest sub-populations, Tanzania.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’. (Eds R. J. Hudson and R. G. White.) pp. 215–238. (CRC Press: Boca Raton, FL.)
Ogutu, J. O., Piepho, H.-P., Dublin, H. T., and Bhola, Ogutu, J. O., Piepho, H.-P., Dublin, H. T., and Bhola, (2008a). El Niño–Southern Oscillation, rainfall, temperature and normalized difference vegetation index fluctuations in the Mara–Serengeti ecosystem. African Journal of Ecology 46, 132–143.
| El Niño–Southern Oscillation, rainfall, temperature and normalized 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 |
Ogutu, J. O., Owen-Smith, N., Piepho, H.-P., Kuloba, B., and Endebe, J. (2012). Dynamics of ungulates in relation to climatic and land use changes in an insularized African savanna ecosystem. Biodiversity and Conservation 21, 1033–1053.
| Dynamics of ungulates in relation to climatic and land use changes in an insularized African savanna ecosystem.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.)
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 |
Pekins, P. J., Smith, K. S., and Mautz, W. W. (1998). The energy costs of gestation in white-tailed deer. Canadian Journal of Zoology 76, 1091–1097.
| The energy costs of gestation in white-tailed deer.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 |
Pettorelli, N., Weladji, R. B., Holand, Ø., Mysterud, A., Breie, H., and Stenseth, N. C. (2005). The relative role of winter conditions: linking climate and landscape-scale plant phenology to alpine reindeer body mass. Biology Letters 1, 24–26.
| The relative role of winter conditions: linking climate and landscape-scale plant phenology to alpine reindeer body mass.Crossref | GoogleScholarGoogle Scholar | 17148119PubMed |
Pettorelli, N., Pelletier, F., von Hardenberg, A., Festa-Bainchet, M., and Côté, S. D. (2007). Early onset of vegetation growth vs rapid green-up: impacts on juvenile mountain ungulates. Ecology 88, 381–390.
| Early onset of vegetation growth vs rapid green-up: impacts on juvenile mountain ungulates.Crossref | GoogleScholarGoogle Scholar | 17479756PubMed |
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., and Forchammer, M. C. (2008). Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Transactions of the Royal Society of London B 363, 2369–2375.
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 |
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.)
Rachlow, J. L., and Bowyer, R. T. (1991). Interannual variation in timing and synchrony of parturition in Dall’s sheep. Journal of Mammalogy 72, 487–492.
| Interannual variation in timing and synchrony of parturition in Dall’s sheep.Crossref | GoogleScholarGoogle Scholar |
Risenhoover, K., and Bailey, J. (1988). Growth rates and birthing period of bighorn sheep in low-elevation environments in Colorado. Journal of Mammalogy 69, 592–597.
| Growth rates and birthing period of bighorn sheep in low-elevation environments in Colorado.Crossref | GoogleScholarGoogle Scholar |
Rodgers, W. A. (1984). Warthog ecology in east Tanzania. Mammalia 48, 327–350.
| Warthog ecology in east Tanzania.Crossref | GoogleScholarGoogle Scholar |
Rosser, A. M. (1989). Environmental and reproductive seasonality of puku, Kobus vardoni, in Luanga Valley, Zambia. African Journal of Ecology 27, 77–88.
| Environmental and reproductive seasonality of puku, Kobus vardoni, in Luanga Valley, Zambia.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 |
Sekulic, R. (1978). Seasonality of reproduction in the sable antelope. East African Wildlife Journal 16, 177–182.
| Seasonality of reproduction in the sable antelope.Crossref | GoogleScholarGoogle Scholar |
Servanty, S., Gaillard, J.-M., Toïgo, C., Brandt, S., and Baubet, E. (2009). Pulsed resources and climate-induced variation in the reproductive traits of wild boar under high hunting pressure. Journal of Animal Ecology 78, 1278–1290.
| Pulsed resources and climate-induced variation in the reproductive traits of wild boar under high hunting pressure.Crossref | GoogleScholarGoogle Scholar |
Simon, N. (1962). ‘Between the Sunlight and the Thunder: the Wild Life of Kenya.’ (Collins: London.)
Sinclair, A. R. E. (1977). ‘The African Buffalo.’ (University of Chicago Press: Chicago, IL.)
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., Van Zyl, J. H., and Van Heerden, J. A. H. (1973). The effect of season on reproduction in the black wildebeest and red hartebeest in South Africa. Journal of Reproduction and Fertility 19, 101–110.
| 1:STN:280:DyaE2c7ivVWhtg%3D%3D&md5=1812bf3369eb993f99ec2b52c9292661CAS | 4522365PubMed |
Skinner, J. D., Van Zyl, J. H., and Oates, L. C. (1974). The effect of season on the breeding cycle of plains antelope of the western Transvaal highveld. Journal of South African Wildlife Management Association 4, 15–23.
Skinner, D. C., Richter, T. A., Malpaux, B., and Skinner, J. D. (2001). Annual ovarian cycles in an aseasonal breeder, the Springbok (Antidorcas marsupialis). Biology of Reproduction 64, 1176–1182.
| Annual ovarian cycles in an aseasonal breeder, the Springbok (Antidorcas marsupialis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1aru7s%3D&md5=207c5d27ff010ce7a476fc6dc1d7c063CAS | 11259265PubMed |
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 |
Smithers, R. H. N. (1983) ‘The Mammals of the Southern African Subregion.’ (University of Pretoria: Pretoria.)
Spinage, C. A. (1969). Reproduction in the Uganda defassa waterbuck, Kobus defassa ugandae Neumann. Journal of Reproduction and Fertility 18, 445–457.
| Reproduction in the Uganda defassa waterbuck, Kobus defassa ugandae Neumann.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M3hsVGmtg%3D%3D&md5=a05767bcbc68e4c6f801e8fd2785b71aCAS | 5788217PubMed | 5788217PubMed |
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 |
Stearns, S. C. (1992). ‘The Evolution of Life Histories.’ (Oxford University Press: 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. Ecology 90, 2057–2067.
| Capital breeding and income breeding: their meaning, measurement and worth.Crossref | GoogleScholarGoogle Scholar | 19739368PubMed |
Talbot, L. M., and Talbot, M. H. (1963). ‘The Wildebeest in Western Maasailand, East Africa.’ Wildlife Monographs. No. 12. (The Wildlife Society: Washington, DC.)
Thompson, R. W., and Turner, J. C. (1982). Temporal geographic variation in the lambing season of bighorn sheep. Canadian Journal of Zoology 60, 1781–1793.
| Temporal geographic variation in the lambing season of bighorn sheep.Crossref | GoogleScholarGoogle Scholar |
Tolsma, D. J., Ernst, W. H. O., Verweij, R. A., and Vooijs, R. (1987). Seasonal variation of nutrient concentrations in a semi-arid savanna ecosystem in Botswana. Journal of Ecology 75, 755–770.
| Seasonal variation of nutrient concentrations in a semi-arid savanna ecosystem in Botswana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjs1OmtQ%3D%3D&md5=dd4b47e7b2ba2fc18931646ea027029dCAS |
Weladji, R. B., and Holand, Ø. (2003). Global climate change and reindeer: effects of winter weather on the autumn weight and growth of calves. Oecolgia 136, 317–323.
| Global climate change and reindeer: effects of winter weather on the autumn weight and growth of calves.Crossref | GoogleScholarGoogle Scholar |
Williamson, D. T. (1991). Condition, growth and reproduction in female red lechwe (Kobus leche leche Gray 1850). African Journal of Ecology 29, 105–117.
| Condition, growth and reproduction in female red lechwe (Kobus leche leche Gray 1850).Crossref | GoogleScholarGoogle Scholar |
Wilson, V. J. (1969). The large mammals of the Matapos National Park. Arnoldia Rhodeia 4, 1–32.
Wilson, D. E., and Hirst, S. M. (1977).’ Ecology and Factors Limiting Roan and Sable Antelope Populations in South Africa.’ Wildlife Monographs No 54. (The Wildlife Society: Washington, DC.)
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 | 1:CAS:528:DC%2BD2sXis1Oktr4%3D&md5=0d938d7e3124632bbdd90e051a09bb19CAS | 17320085PubMed | 17320085PubMed |
Wronski, T., Lerp, H., and Ismail, K. (2011). Reproductive biology and life history traits of Arabian oryx (Oryx leucoryx) founder females reintroduced to Mahazat as-Sayd, Saudi Arabia. Mammalian Biology-Zeitschrift für Säugetierkunde 76, 506–511.
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 | 22780447PubMed |