Reproductive seasonality in captive wild ruminants: Implications for biogeographical adaptation, photoperiodic control, and life history

Biological Reviews

Volumn 87, Issue 4, 2012, Pages 965-990

  Zerbe, Philipp ^a   Clauss, Marcus ^a   Codron, Daryl ^a,b,c,d   Bingaman Lackey, Laurie ^e   Rensch, Eberhard ^a   Streich, Jürgen W ^f   Hatt, Jean Michel ^a   Müller, Dennis W H ^a,g  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b NATIONAL MUSEUM   (South Africa)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d UNIVERSITY OF COLORADO   (United States)

^e International Species Information System   (United States)

^f LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^g National Park 'Bavarian Forest'   (Germany)

Author keywords

Bergmann's rule; Gestation; Phenology; Photoperiodism; Rensch's rule; Reproduction; Seasonality

Indexed keywords

ADAPTATION; ANIMAL; ARTICLE; BOVIDS; FEMALE; MALE; PHOTOPERIODICITY; PHYSIOLOGY; REPRODUCTION; SEASON; ZOO ANIMAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, ZOO; FEMALE; MALE; PHOTOPERIOD; REPRODUCTION; RUMINANTS; SEASONS;

ANIMALIA; ANTIDORCAS MARSUPIALIS; BOVIDAE;

EID: 84867142926     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/j.1469-185X.2012.00238.x     Document Type: Article

References (170)

1. Aanes, R. & Andersen, R. (1996). The effects of sex, time of birth, and habitat on the vulnerability of roe deer fawns to red fox predation. Canadian Journal of Zoology 74, 1857-1865.
2. Abouheif, E. & Fairbairn, D. J. (1997). A comparative analysis of allometry for sexual size dimorphism: assessing Rensch's rule. American Naturalist 149, 540-562.
3. Adams, L. G. & Dale, B. W. (1998). Timing and synchrony of parturition in Alaskan caribou. Journal of Mammalogy 79, 287-294.
4. Adams, L. G., Singer, F. J. & Dale, B. W. (1995). Caribou calf morality in Denali National Park, Alaska. Journal of Wildlife Management 59, 584-594.
5. Ahrestani, F. S., Van Langevelde, F., Heitkönig, I. M. A. & Prins, H. H. T. (2011). 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 (doi: 10.1111/j.1600-0706.2011.20244.x).
6. Alexander, R. D., Hoogland, J. L., Howard, R. D., Noonan, K. M. & Sherman, P. W. (1979). Sexual dimorphism and breeding system in pinnipeds, ungulates, primates, and humans. In Evolutionary Biology and Human Social Behavior: An Anthropological Perspective (eds N. A. Chagnon and W. Irons), pp. 402-435. Duxbury, North Scituate.
7. Asher, G. W., Monfort, S. L. & Wemmer, C. (1999). Comparative reproductive function in cervids: implications for management of farm and zoo populations. Journal of Reproduction and Fertility Supplement 54, 143-156.
8. Ashton, K. G., Tracy, M. C. & De Queiroz, A. (2000). Is Bergmann's rule valid for mammals? American Naturalist 156, 390-415.
9. Baker, R. H. (2002). Comparative methods. In Techniques in Molecular Systematics and Evolution (eds R. DeSalle, G. Giribet and W. Wheeler), pp. 146-161. Birkhäuser Verlag, Basel.
10. Barrette, C. (1987). The comparative behavior and ecology of Chevrotains, Musk deer, and morphologically conservative deer. In Biology and Management of the Cervidae (ed. C. M. Wemmer), pp. 200-213. Smithsonian Institution Press, Washington.
11. Beja-Pereira, A., Caramelli, D., Lalueza-Fox, C., Vernesi, C., Ferrand, N., Casoli, A., Goyache, F., Royo, L. J., Conti, S., Lari, M., Martini, A., Ouragh, L., Magid, A., Atash, A., Zsolnai, A., Boscato, P., Triantaphylidis, C., Ploumi, K., Sineo, L., Mallegni, F., Taberlet, P., Erhardt, G., Sampietro, L., Bertranpetit, J., Barbujani, G., Luikart, G. & Bertorelle, G. (2006). The origin of European cattle: evidence from modern and ancient DNA. Proceedings of the National Academy of Sciences 103, 8113-8118.
12. Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L. & Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507-512.
13. Bonenfant, C., Loe, L. E., Mysterud, A., Langvatn, R., Stenseth, N. C., Gaillard, J.-M. & Klein, F. (2004). Multiple causes of sexual segregation in European red deer enlightenments from varying breeding phenology at high and low latitude. Proceedings of the Royal Society B 271, 883-892.
14. Bos, H. & Van der Mey, G. J. W. (1980). Length of gestation periods of horses and ponies belonging to different breeds. Livestock Production Science 7, 181-187.
15. Bowyer, R. T. (1991). Timing of parturition and lactation in southern mule deer. Journal of Mammalogy 72, 138-145.
16. Bowyer, R. T., Van Ballenberghe, V. & Kie, J. G. (1998). Timing and synchrony of parturition in Alaskan moose: long-term versus proximal effects of climate. Journal of Mammalogy 79, 1332-1344.
17. Bradshaw, W. E. & Holzapfel, C. M. (2007). Evolution of animal photoperiodism. Annual Reviews of Ecology, Evolution, and Systematics 38, 1-25.
18. Brand, D. J. (1963). Records of mammals bred in the national zoological gardens of South Africa during the period 1908 to 1960. Proceedings of the Zoological Society of London 140, 617-659.
19. Brinklow, B. R. & Loudon, A. S. (1993). Gestation period in the Père David's deer (Elaphurus davidianus): evidence for embryonic diapause or delayed development. Reproduction, Fertility and Development 5, 567-575.
20. Bro-Jørgensen, J. (2008). Dense habitats selecting for small body size: a comparative study on bovids. Oikos 117, 729-737.
21. Bronson, F. H. (1985). Mammalian reproduction: an ecological perspective. Biology of Reproduction 32, 1-26.
22. Bronson, F. H. (1989). Mammalian Reproductive Biology University of Chicago Press, Chicago.
23. Bronson, F. H. (2009). Climate change and seasonal reproduction in mammals. Philosophical Transactions of the Royal Society B 364, 3331-3340.
24. Bubenik, G., Reyes, E., Schams, D., Lobos, A. & Bartoš, L. (2000). Pudu, the smallest deer of the world: 10 years of endocrine studies of Southern Pudu (Pudu puda) in Chile. Zeitschrift für Jagdwissenschaft 46, 129-138.
25. Buechner, H. K. (1950). Life history, ecology, and range use of the pronghorn antelope in Trans-Pecos Texas. American Midland Naturalist 43, 257-354.
26. Bunnell, F. L. (1982). The lambing period of Mountain sheep: synthesis, hypotheses, and tests. Canadian Journal of Zoology 60, 1-14.
27. Burthe, S., Butler, A., Searle, K. R., Hall, S. J. G., Thackeray, S. J. & 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.
28. Caughley, G. (1971). The season of births for northern-hemisphere ungulates in New Zealand. Mammalia 35, 204-219.
29. Caughley, G. & Caughley, J. (1974). Estimating median date of birth. The Journal of Wildlife Management 38, 552-556.
30. Chemineau, P., Daveau, A., Cognie, Y., Aumont, G. & Chesneau, D. (2004). Seasonal ovulatory activity exists in tropical Creole female goats and Black Belly ewes subjected to a temperate photoperiod. BMC Physiology 4, 12.
31. Chemineau, P., Guillaume, D., Migaud, M., Thiéry, J. C., Pellicer-Rubio, M. T. & Malpaux, B. (2008). Seasonality of reproduction in mammals: intimate regulatory mechanisms and practical implications. Reproduction in Domestic Animals 43, 40-47.
32. Clauss, M., Hume, I. D. & Hummel, J. (2010). Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4, 979-992.
33. Clauss, M., Kaiser, T. & Hummel, J. (2008). The morphophysiological adaptations of browsing and grazing mammals. In The Ecology of Browsing and Grazing (eds I. J. Gordon and H. H. T. Prins), pp. 47-88. Springer, Heidelberg.
34. Clements, M. N., Clutton-Brock, T. H., Albon, S. D., Pemberton, J. M. & Kruuk, L. E. B. (2011). Gestation length variation in a wild ungulate. Functional Ecology 25, 691-703.
35. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. (1983). The costs of reproduction to Red deer hinds. Journal of Animal Ecology 52, 367-383.
36. Codron, D., Brink, J. S., Rossouw, L. & Clauss, M. (2008a). The evolution of ecological specialization in southern African ungulates: competition- or physical environmental turnover? Oikos 117, 344-353.
37. Codron, D., Brink, J. S., Rossouw, L., Clauss, M., Codron, J., Lee-Thorp, J. A. & Sponheimer, M. (2008b). Functional differentiation of African grazing ruminants: an example of specialized adaptations to very small changes in diet. Biological Journal of the Linnaean Society 94, 755-764.
38. Codron, D. & Clauss, M. (2010). Rumen physiology constrains diet niche: linking digestive physiology and food selection across wild ruminant species. Canadian Journal of Zoology 88, 1129-1138.
39. Côté, S. D. & Festa-Bianchet, M. (2001). Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127, 230-238.
40. Dardene, H. (2012). Melatonin-dependent timing of seasonal reproduction by the Pars tuberalis: pivotal roles for long daylengths and thyroid hormones. Journal of Neuroendocrinology 24, 249-266.
41. Dasmann, R. F. & Mossman, A. S. (1962). Reproduction in some ungulates in Southern Rhodesia. Journal of Mammalogy 43, 533-537.
42. Dauphiné, T. C. & McClure, R. L. (1974). Synchronous mating in Canadian barren-ground caribou. Journal of Wildlife Management 38, 54-66.
43. Deng, T., Wang, X., Fortelius, M., Li, Q., Wang, Y., Tseng, Z. J., Takeuchi, G. T., Saylor, J. E., Säilä, L. K. & Xie, G. (2011). Out of Tibet: pliocene woolly rhino suggests high-plateau origin of ice age megaherbivores. Science 333, 1285.
44. Dittrich, L. (1970). Beitrag zur Fortpflanzungsbiologie afrikanischer Antilopen im Zoologischen Garten. Der Zoologische Garten NF 39, 16-40.
45. Estes, R. D. (1976). The significance of breeding synchrony in the Wildebeest. African Journal of Ecology 14, 135-152.
46. Fairall, N. (1968). The reproductive season of some mammals in the Kruger National Park. Zoologica Africana 3, 189-210.
47. Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 1-15.
48. Festa-Bianchet, M. (1988). Birthdate and survival in Bighorn lambs (Ovis canadensis). Journal of Zoology 214, 653-661.
49. Fisher, D. O., Blomberg, S. P. & Owens, I. P. F. (2002). Convergent maternal care strategies in ungulates and macropods. Evolution 56, 167-176.
50. Fletcher, T. J. (1974). The timing of reproduction in Red deer (Cervus elaphus) in relation to latitude. Journal of Zoology 172, 363-367.
51. Flood, P. F. & Tedesco, S. C. (1997). Relationship between conception date and latitude in muskoxen. Rangifer 17, 25-30.
52. Flower, S. S. (1932). Notes on the recent mammals of Egypt, with a list of the species recorded from that kingdom. Proceedings of the Royal Society of London 102, 369-450.
53. Flydal, K. & Reimers, E. (2002). Relationship between calving time and physical condition in three wild Reindeer (Rangifer tarandus) populations in southern Norway. Wildlife Biology 8, 145-151.
54. Forsythe, W. C., Rykiel, E. J., Stahl, R. S., Wu, H.-I. & Schoolfield, R. M. (1995). A model comparison for daylength as a function of latitude and day of year. Ecological Modelling 80, 87-95.
55. Geist, V. (1974a). On the Relationship of Ecology and Behavior in the Evolution of Ungulates: Theoretical Considerations. IUCN, Morges.
56. Geist, V. (1974b). On the relationship of social evolution and ecology in ungulates. American Zoologist 14, 205-220.
57. Geist, V. (1987). On speciation in Ice Age mammals, with special reference to cervids and caprids. Canadian Journal of Zoology 65, 1067-1084.
58. Giuffra, E., Kijas, J. M. H., Amarger, V., Carlborg, O., Jeon, J. T. & Andersson, L. (2000). The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 154, 1785-1791.
59. Green, W. C. H. & Rothstein, A. (1993). Asynchronous parturition in bison: implications for the hider-follower-dichotomy. Journal of Mammalogy 74, 920-925.
60. Gregg, M. A., Bray, M., Kilbride, K. M. & Dunbar, M. R. (2001). Birth synchrony and survival of pronghorn fawns. Journal of Wildlife Management 65, 19-24.
61. Hall-Martin, A. J., Skinner, J. D. & Van Dyk, J. M. (1975). Reproduction in the giraffe in relation to some environmental factors. African Journal of Ecology 13, 237-248.
62. Hamilton, W. J. & Blaxter, K. L. (1980). Reproduction in farmed red deer. 1. Hind and stag fertility. Journal of Agricultural Science 95, 261-273.
63. Hazlerigg, D. G. & Lincoln, G. A. (2011). Hypothesis: cyclical histogenesis is the basis of circannual timing. Journal of Biological Rhythms 26, 471-485.
64. Hazlerigg, D. G. & Loudon, A. (2008). New insights into ancient seasonal life timers. Current Biology 18, R795-R804.
65. Hodges, J. K., Bevan, D. J., Celma, M., Hearn, J. P., Jones, D. M., Kleiman, D. G., Knight, J. A. & Moore, H. D. M. (1984). Aspects of the reproductive endocrinology of the female Giant panda (Ailuropoda melanoleuca) in captivity with special reference to the detection of ovulation and pregnancy. Journal of Zoology 203, 253-267.
66. Hut, R. A. & Beersma, D. G. M. (2011). Evolution of time-keeping mechanisms: early emergence and adaptation to photoperiod. Philosophical Transactions of the Royal Society B 366, 2141-2154.
67. Ims, R. A. (1990a). On the adaptive value of reproductive synchrony as a predator swamping strategy. American Naturalist 136, 485-498.
68. Ims, R. A. (1990b). The ecology and evolution of reproductive synchrony. Trends in Ecology and Evolution 5, 135-140.
69. Isaac, J. L. (2005). Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal Review 35, 101-115.
70. Jabbour, H. N., Hayssen, V. & Bruford, M. W. (1997). Conservation of deer: contributions from molecular biology, evolutionary ecology, and reproductive physiology. Journal of Zoology 243, 461-484.
71. Jafar, S. M., Chapman, A. B. & Casida, L. E. (1950). Causes of variation in length of gestation in dairy cattle. Journal of Animal Science 9, 593-601.
72. Jarman, P. J. (1983). Mating system and sexual dimorphism in large, terrestrial, mammalian herbivores. Biological Reviews 58, 485-520.
73. Jones, K. E., Bielby, J., Cardillo, M., Fritz, S. A., O'Dell, J., Orme, C. D. L., Safi, K., Sechrest, W., Boakes, E. H., Carbone, C., Connolly, C., Cutts, M. J., Foster, J. K., Grenyer, R., Habib, M., Plaster, C. A., Price, S. A., Rigby, E. A., Rist, J., Teacher, A., Bininda-Emonds, O. R. P., Gittleman, J. L., Mace, G. M., Purvis, A. & Michener, W. K. (2009). PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648.
74. Kiltie, R. A. (1984). Seasonality, gestation time, and large mammal extinctions. In Quaternary Extinctions: A Prehistoric Revolution (eds P. S. Martin and R. G. Klein), pp. 299-314. University of Arizona Press, Tucson.
75. Kiltie, 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.
76. Kirkwood, J. K., Gaskin, C. D. & Markham, J. (1987). Perinatal mortality and season of birth in captive wild ungulates. Veterinary Record 120, 386-390.
77. Körner, C. (2007). The use of 'altitude' in ecological research. Trends in Ecology & Evolution 22, 569-574.
78. Lane, J. E., Boutin, S., Speakman, J. R. & Humphries, M. M. (2010). Energetic costs of male reproduction in a scramble competition mating system. Journal of Animal Ecology 79, 27-34.
79. Lent, P. C. (1974). Mother-infant relationships in ungulates. In The behavior of Ungulates and its Relation to Management (eds V. Geist and F. Walther), pp. 14-55. International Union for the Conservation of Nature and Natural Resources, Morges.
80. Leuthold, W. & Leuthold, B. M. (1975). Temporal patterns of reproduction in ungulates of Tsavo East National Park, Kenya. African Journal of Ecology 13, 159-169.
81. Lincoln, G. A. (1985). Seasonal breeding in deer. In Biology of Deer Production (Volume 22, eds P. F. Fennessey and K. R. Drew), pp. 165-180. Bulletin of the Royal Society of New Zealand, Wellington.
82. Lincoln, G. A., Clarke, I. J., Hut, R. A. & Hazlerigg, D. G. (2006). Characterizing a mammalian circannual pacemaker. Science 314, 1941-1944.
83. Lincoln, G. A. & Short, R. V. (1980). Seasonal breeding: nature's contraceptive. Recent Progress in Hormone Research 36, 1-53.
84. Linnell, J. D. C. & Andersen, R. (1998). Timing and synchrony of birth in a hider species, the Roe deer (Capreolus capreolus). Journal of Zoology 244, 497-504.
85. Loe, L. E., Bonenfant, C., Mysterud, A., Gaillard, J.-M., Langvatn, R., Klein, F., Calenge, C., Ergon, T., Pettorelli, N. & Stenseth, N. C. (2005). Climate predictability and breeding phenology in red deer: timing and synchrony of rutting and calving in Norway and France. Journal of Animal Ecology 74, 579-588.
86. Loison, A., Gaillard, J.-M., Pélabon, C. & Yoccoz, N. G. (1999). What factors shape sexual size dimorphism in ungulates? Evolutionary Ecology Research 1, 611.
87. Maddison, W. P. & Maddison, D. R. (2006). Mesquite: a modular system for evolutionary analysis. Available at http://mesquiteproject.org; accessed on 1 December 2010.
88. Marshall, F. H. A. (1937). On the change over in the oestrous cycle in animals after transference across the equator, with further observations on the incidence of the breeding seasons and the factors controlling sexual periodicity. Proceedings of the Royal Society of London B 122, 413-428.
89. Martins, E. (2004). COMPARE, Version 4.6. Computer Programs for the Statistical Analysis of Comparative Data Department of Biology, Indiana University, Bloomington, Distributed by the author at http://compare.bio.indiana.edu/; accessed on 1 August 2005.
90. Martins, E. P. & Hansen, T. F. (1997). Phylogenesis and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 149, 646-667.
91. Masui, M., Hiramatsu, H., Nose, N., Nakazato, R., Sagawa, Y., Tajima, H. & Saito, K. (1989). Successful artificial insemination in the Giant panda (Ailuropoda melanoleuca) at Ueno Zoo. Zoo Biology 8, 17-26.
92. Matsubayashi, H., Bosi, E. & Kohshima, S. (2003). Activity and habitat use of Lesser Mouse-Deer (Tragulus javanicus). Journal of Mammalogy 84, 234-242.
93. McGinnes, B. S. & Downing, R. L. (1977). Factors affecting the peak of White-tailed deer fawning in Virginia. Journal of Wildlife Management 41, 715-719
94. Meiri, S. & Dayan, T. (2003). On the validity of Bermann's rule. Journal of Biogeography 30, 331-351.
95. Meissner, H. H., Zacharias, P. J. K. & O'Reagain, P. J. (1999). Forage quality (feed value). In Veld Management in South Africa (ed. N. M. Tainton), pp. 139-168. University of Natal Press, Pietermaritzburg.
96. Meng, X., Yang, Q., Feng, Z., Xia, L., Jiang, Y. & Wang, P. (2003). Timing and synchrony of parturition in Alpine musk deer (Moschus sifanicus). Folia Zoologica 52, 39-50.
97. Miquelle, D. G. (1990). Why don't bull moose eat during the rut? Behavioral Ecology and Sociobiology 27, 145-151.
98. Mitchell, B. & Lincoln, G. A. (1973). Conception dates in relation to age and condition in two populations of red deer in Scotland. Journal of Zoology 171, 141-152.
99. Moe, S. R., Rutina, L. P. & Du Toit, J. T. (2007). Trade-off between resource seasonality and predation risk explains reproductive chronology in impala. Journal of Zoology 273, 237-243.
100. Monfort, S. L., Wemmer, C. M., Kepler, T. H., Bush, M., Brown, J. L. & Wildt, D. E. (1990). Monitoring ovarian function and pregnancy in Eld's deer (Cervus eldi) by evaluating urinary steroid metabolite excretion. Journal of Reproduction and Fertility 88, 271-281.
101. Montgomery, G. W., Scott, I. C. & Hudson, N. (1985). An interaction between season of calving and nutrition on the resumption of ovarian cycles in post-partum beef cattle. Journal of Reproduction and Fertility 73, 45-50.
102. Mooney, H. A. & Billings, W. D. (1961). Comparative physiological ecology of arctic and alpine populations of Oxyria digyna. Ecological Monographs 31, 1-29.
103. Moyes, K., Nussey, D. H., Clements, M. N., Guinness, F. E., Morris, A., Morris, S., Pemberton, J. M., Kruuk, L. E. B. & 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.
104. Müller, D. W. H., Caton, J., Codron, D., Schwarm, A., Lentle, R., Streich, W. J., Hummel, J. & Clauss, M. (2011a). Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comparative Biochemistry and Physiology A 160, 207-220.
105. Müller, D. W. H., Zerbe, P., Codron, D., Clauss, M. & Hatt, J. M. (2011b). A long life among ruminants: giraffids and other special cases. Schweizer Archiv für Tierheilkunde 153, 515-519.
106. Nievergelt, B. (1966). Unterschiede in der Setzzeit beim Alpensteinbock (Capra ibex). Revue Suisse de Zoologie 73, 446-454.
107. Nievergelt, B. (1974). A comparison of rutting behaviour and grouping in the Ethiopian and Alpine ibex. In The Behavior of Ungulates and its Relation to Management (eds V. Geist and F. Walther), pp. 324-340. International Union for the Conservation of Nature and Natural Resources, Morges.
108. Nowak, R. M. (1991). Chevrotains, or mouse deer. Walker's Mammals of the World (Volume 2), pp. 1359-1362. Johns Hopkins University Press, Baltimore.
109. O'Donoghue, M. & Boutin, S. (1995). Does reproductive synchrony affect juvenile survival rates of northern mammals? Oikos 74, 115-121.
110. Ogutu, J., Piepho, H.-P., Dublin, H., Bhola, N. & Reid, R. (2010). Rainfall extremes explain interannual shifts in timing and synchrony of calving in topi and warthog. Population Ecology 52, 89-102.
111. Ogutu, J., Piepho, H.-P., Dublin, H., Bhola, N. & Reid, R. (2011). Dynamics of births and juvenile recruitment in Mara-Serengeti ungulates in relation to climatic and land use changes. Population Ecology 53, 195-213.
112. Ortavant, R., Pelletier, J., Ravault, J. P., Thimonier, J. & Volland-Nail, P. (1985). Photoperiod: main proximal and distal factor of the circannual cycle of reproduction in farm mammals. Oxford Reviews of Reproductive Biology 7, 305-345.
113. Owen-Smith, N. (1988). Megaherbivores-The Influence of Very Large Body Size on Ecology. Cambridge University Press, Cambridge.
114. Owen-Smith, N. (2002). Adaptive Herbivore Ecology. From Resources to Populations in Variable Environments Cambridge University Press, Cambridge.
115. Owen-Smith, N. & Cooper, S. M. (1989). Nutritional ecology of a browsing ruminant, the kudu (Tragelaphus strepsiceros), through the seasonal cycle. Journal of Zoology 219, 29-43.
116. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877-884.
117. Panzacchi, M., Linnell, J. D. C., Odden, J., Odden, M. & Andersen, R. (2008). When a generalist becomes a specialist: patterns of red fox predation on roe deer fawns under contrasting conditions. Canadian Journal of Zoology 86, 116-126.
118. Paré, P., Barrette, C. & Prescott, J. (1996). Seasonal reproduction of captive Himalayan tahrs (Hemitragus jemlahicus) in relation to latitude. Journal of Mammalogy 77, 826-832.
119. Pedrosa, S., Uzun, M., Arranz, J.-J., Gutiérrez-Gil, B., San Primitivo, F. & Bayón, Y. (2005). Evidence of three maternal lineages in near eastern sheep supporting multiple domestication events. Proceedings of the Royal Society B: Biological Sciences 272, 2211-2217.
120. Pelt, F. L. (1967). Remarks on breeding seasons of some Artiodactyla in captivity. Der Zoologische Garten NF 34, 293-296.
121. Penfold, L. M. (2005). Reproductive physiology and artificial insemination studies in wild and captive Gerenuk (Litocranius walleri walleri). Reproduction, Fertility and Development 17, 707.
122. Pérez-Barberìa, F. J., Gordon, I. J. & Nores, C. (2001). Evolutionary transitions among feeding styles and habitats in ungulates. Evolutionary Ecology Research 3, 221-230.
123. Pérez-Barberìa, F. J., Gordon, I. J. & Pagel, M. (2002). The origins of sexual dimorphism in body size in ungulates. Evolution 56, 1276-1285.
124. Piening Schuler, Y., Hammer, C., Clauss, C. & Hammer, S. (2009). Birth seasonality in captive bovids at the Al Wabra Wildlife Preservation (AWWP), Qatar. In Proceedings of the International Conference on Diseases of Zoo and Wild Animals, pp. 1297-1303. Beekse Bergen, The Netherlands.
125. Polák, J. & Frynta, D. (2009). Sexual size dimorphism in domestic goats, sheep, and their wild relatives. Biological Journal of the Linnaean Society 98, 872-883.
126. Polák, J. & Frynta, D. (2010). Patterns of sexual size dimorphism in cattle breeds support Rensch's rule. Evolutionary Ecology 24, 1255-1266.
127. Post, E. (2003). Timing of reproduction in large mammals. In Phenology: An Integrative Environmental Science (ed. M. D. Schwartz), pp. 437-449. Kluwer Academic Publishers, Dordrecht.
128. Post, E., Bøving, P. S., Pedersen, C. & MacArthur, M. A. (2003). Synchrony between caribou calving and plant phenology in depredated and non-depredated populations. Canadian Journal of Zoology 81, 1709-1714.
129. Post, E. & Forchhammer, M. C. (2008). Climate changes reduces reproductive success of an Arctic herbivore through trophic mismatch. Philosophical Transactions of the Royal Society B 363, 2369-2375.
130. Post, E., Pedersen, C., Wilmers, C. C. & Forchhammer, M. C. (2008). Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proceedings of the Royal Society B 275, 2005-2013.
131. Powlesland, R. G., Lloyd, B. D., Best, H. A. & Merton, D. V. (1992). Breeding biology of the Kakapo (Strigops habroptilus) on Stewart Island, New Zealand. Ibis 135, 361-373.
132. Ptak, G. E., Tacconi, E., Czernik, M., Toschi, P., Modlinski, J. A. & Loi, P. (2012). Embryonic diapause is conserved across mammals. PLoS ONE 7, e33027.
133. Rachlow, J. L. & Bowyer, R. T. (1991). Intraannual variation in timing and synchrony of parturition in Dall's sheep. Journal of Mammalogy 72, 487-492.
134. Ralls, K., Kranz, K. & Lundrigan, B. (1986). Mother-young relationships in captive ungulates: variability and clustering. Animal Behaviour 34, 134-145.
135. Ransom, A. B. (1966). Breeding seasons of white-tailed deer in Manitoba. Canadian Journal of Zoology 44, 59-62.
136. Rhind, S. M., Archer, Z. A. & Adam, C. L. (2002). Seasonality of food intake in ruminants: recent developments in understanding. Nutrition Research Reviews 15, 43-65.
137. Rice, C. G. (1988). Reproductive biology of Nilgiri tahr (Hemitragus hylocrius). Journal of Zoology 214, 269-284.
138. Robbins, C. T. & Robbins, B. L. (1979). Fetal and neonatal growth patterns and maternal reproductive effort in ungulates and subungulates. American Naturalist 114, 101-116.
139. Rohlf, F. (2001). Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55, 2143-2160.
140. Ruf, T., Fietz, J., Schlund, W. & Bieber, C. (2006). High survival in poor years: life history tactics adapted to mast seeding in the edible Dormouse. Ecology 87, 372-381.
141. Rutberg, A. T. (1984). Birth synchrony in American bison (Bison bison): response to predation or season? Journal of Mammalogy 65, 418-423.
142. Rutberg, A. T. (1987). Adaptive hypotheses of birth synchrony in ruminants: an interspecific test. American Naturalist 130, 692.
143. Ryan, S. J., Knechtel, C. U. & Getz, W. M. (2007). Ecological cues, gestation length, and birth timing in African buffalo (Syncerus caffer). Behavioral Ecology 18, 635-644.
144. Sadleir, R. M. F. S. (1969). The Ecology of Reproduction in Wild and Domestic Mammals Methuen & Co, London.
145. Saether, B.-E., Andersen, R., Hjeljord, O. & Heim, O. (1996). Ecological correlates of regional variation in life history of the Moose (Alces alces). Ecology 77, 1493-1500.
146. Santiago-Moreno, J., Gómez-Brunet, A., Toledano-Díaz, A., Picazo, R., Gonzalez-Bulnes, A. & López-Sebastián, A. (2006). Seasonal endocrine changes and breeding activity in Mediterranean wild ruminants. Reproduction in Domestic Animals 41, 72-81.
147. Short, R. V. & Hay, M. F. (1966). Delayed implantation in the roe deer (Capreolus capreolus). In Comparative Biology in Mammals, Symposium of the Zoological Society of London, Vol. 15 (ed. I. W. Rowlands), pp. 173-194. Academic Press, London.
148. Sinclair, A. R., Ludwig, D. & Clark, C. W. (2000a). Conservation in the real world. Science 289, 1875.
149. Sinclair, A. R. E., Mduma, S. A. & Arcese, P. (2000b). What determines phenology and synchrony of ungulate breeding in Serengeti? Ecology 81, 2100-2111.
150. Skinner, J. D., Aarde, R. J. V., Knight, M. H. & Dott, H. M. (1996). Morphometries and reproduction in a population of Springbok Antidorcas marsupialis in the semi-arid southern Kalahari. African Journal of Ecology 34, 312-330.
151. Skinner, J. D., Moss, D. G. & 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.
152. Skinner, D. C., Richter, T. A., Malpaux, B. & Skinner, J. D. (2001). Annual ovarian cycles in an aseasonal breeder, the springbok (Antidorcas marsupialis). Biology of Reproduction 64, 1176-1182.
153. Smith, B. L. & Anderson, S. H. (1998). Juvenile survival and population regulation of the Jackson elk herd. Journal of Wildlife Management 62, 1036-1045.
154. Solounias, N. (2007). Family Giraffidae. In The Evolution of Artiodactyla (ed. D. R. Prothero), pp. 257-277. John Hopkins University Press, Baltimore.
155. Sparks, T. H. & Menzel, A. (2002). Observed changes in seasons: an overview. International Journal of Climatology 22, 1715-1725.
156. Spinage, C. A. (1973). The role of photoperiodism in the seasonal breeding of tropical African ungulates. Mammal Review 3, 71-83.
157. Testa, J. W. (2002). Does predation on neonates inherently select for earlier births? Journal of Mammalogy 83, 699-706.
158. Testa, J. W., Becker, E. F. & Lee, G. R. (2000). Temporal patterns in the survival of twin and single moose calves (Alces alces) in southcentral Alaska. Journal of Mammalogy 81, 162-168.
159. The Duke of Bedford & Marshall, F. H. A. (1942). On the incidence of the breeding season in mammals after transference to a new latitude. Proceedings of the Royal Society of London. Series B: Biological Sciences 130, 396-399.
160. Ungerfeld, R., González-Pensado, S., Bielli, A., Villagrán, M., Olazabal, D. & Pérez, W. (2008). Reproductive biology of the Pampas deer (Ozotoceros bezoarticus): a review. Acta Veterinaria Scandinavica 50, 16.
161. Van Mourik, S. A. & Stelmasiak, T. (1990). Endocrine mechanisms and antler cycles in rusa deer (Cervus timorensis). In Horns, Pronghorns and Antlers (eds G. A. Bubenik and A. B. Bubenik), pp. 265-297. Springer, New York.
162. Verme, L. J. (1965). Reproduction studies on penned White-tailed deer. Journal of Wildlife Management 29, 74-79.
163. Verme, L. J. (1969). Reproductive pattern of White-tailed deer related to nutritional plane. Journal of Wildlife Management 33, 881-887.
164. Verme, L. J. & Ozoga, J. J. (1987). Relationship of photoperiod to puberty in doe fawn white-tailed deer. Journal of Mammalogy 68, 107-110.
165. Weckerly, F. W. (1998). Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. Journal of Mammalogy 79, 33-52.
166. Western, D. (1979). Size, life history and ecology in mammals. African Journal of Ecology 17, 185-204.
167. Wilson, V. J. (2005). Duikers of Africa (Masters of the African forest floor) Zimbi Books, Pretoria.
168. Zeder, M. A. & Hesse, B. (2000). The initial domestication of goats (Capra hircus) in the Zagros Mountains 10, 000 years ago. Science 287, 2254-2257.
169. Zieba, D. A., Klocek, B., Williams, G. L., Romanowicz, K., Boliglowa, L. & Wozniak, M. (2007). In vitro evidence that leptin suppresses melatonin secretion during long days and stimulates its secretion during short days in seasonal breeding ewes. Domestic Animal Endocrinology 33, 358-365.
170. Zuckerman, S. (1952). The breeding seasons of mammals in captivity. Proceedings of the Zoological Society of London 122, 827-950.