Population Ecology

, Volume 52, Issue 1, pp 89–102

Rainfall extremes explain interannual shifts in timing and synchrony of calving in topi and warthog

  • Joseph O. Ogutu
  • Hans-Peter Piepho
  • Holly T. Dublin
  • Nina Bhola
  • Robin S. Reid
Original Article

Abstract

We tested the hypothesis that ungulates time and synchronize births to match gestation and lactation with peak food availability and quality in seasonal environments, using ground counts of topi and warthog conducted over 174 months (July 1989–December 2003) in the Mara–Serengeti ecosystem. During this 15-year period, 2,725 newborn and 45,574 adult female topi and 933 newborn and 7,831 adult warthogs were recorded. Births were distinctly synchronized in both species but far less so than in ungulates in temperate regions. Extreme droughts delayed onset and reduced synchrony of calving and natality rates but high rainfall advanced onset and increased synchrony of calving and natality rates in both species, supporting the seasonality hypothesis. Annual shifts in birth peaks were significantly negatively correlated with the preceding wet season rainfall. Varying the timing and synchrony of births and natality rates are widespread but little understood adaptations of ungulates to climatic extremes. Climate change heightens the need for advancing this understanding because increasing frequency and severity of droughts is likely to decouple phenology of breeding in seasonally breeding ungulates from that in their food plants. Similar studies of African ungulates are either extremely rare or non-existent. New approaches to estimating the time of peak births and its confidence limits and the degree of synchrony of breeding are also presented.

Keywords

Breeding Droughts Floods Mara–Serengeti ecosystem Phenology Ungulates 

Supplementary material

10144_2009_163_MOESM1_ESM.pdf (73 kb)
Appendix A (PDF 72 kb)
10144_2009_163_MOESM2_ESM.pdf (25 kb)
Appendix B (PDF 25 kb)

References

  1. Adams LG, Dale BW (1998) Timing and synchrony of parturition in Alaskan caribou. J Mammal 79:287–294. doi:10.2307/1382865 CrossRefGoogle Scholar
  2. Alexander G (1956) Influences of nutrition upon duration of gestation in sheep. Nature 178:1058–1059. doi:10.1038/1781058a0 CrossRefPubMedGoogle Scholar
  3. Ayalon N (1978) A review of embryonic mortality in cattle. J Reprod Fertil 74:631–636Google Scholar
  4. Berger J (1992) Facilitation of reproductive synchrony by gestation adjustment in gregarious mammals: a new hypothesis. Ecology 73:323–329. doi:10.2307/1938743 CrossRefGoogle Scholar
  5. Boshe JI (1981) Reproductive ecology of the warthog Phacochoerus aethiopicus and its significance for management in the eastern Selous Game Reserve, Tanzania. Biol Conserv 20:37–44. doi:10.1016/0006-3207(81)90059-8 CrossRefGoogle Scholar
  6. Bowyer RT, VanBallenberghe V, Kie JG (1998) Timing and parturition in Alaskan moose: long-term versus proximal effects of climate. J Mammal 79:1332–1344. doi:10.2307/1383025 CrossRefGoogle Scholar
  7. Bro-Jørgensen J (2002) Overt female mate competition and preference for central males in a lekking antelope. Proc Natl Acad Sci USA 99:9290–9293. doi:10.1073/pnas.142125899 CrossRefPubMedGoogle Scholar
  8. Bro-Jørgensen J (2003) No peace for estrous topi cows on leks. Behav Ecol 14:521–525. doi:10.1093/beheco/arg026 CrossRefGoogle Scholar
  9. Brown CE (1936) Rearing wild animals in captivity and gestation periods. J Mammal 17:10–13. doi:10.2307/1374541 CrossRefGoogle Scholar
  10. Buechner HK (1960) The bighorn sheep in the United States, its past, present and future. Wildlife Monograph 4. The Wildlife Society, Washington, D.C.Google Scholar
  11. Bunnell FL (1982) The lambing period of mountain sheep: synthesis, hypothesis, and tests. Can J Zool 60:1–14. doi:10.1139/z82-001 CrossRefGoogle Scholar
  12. Byers JA, Hogg JT (1995) Environmental effects on parental growth rate in pronghorn and bighorn: further evidence for energy constraint on sex-biased maternal expenditure. Behav Ecol 6:451–457. doi:10.1093/beheco/6.4.451 CrossRefGoogle Scholar
  13. Child G, Roth HH, Kerr M (1968) Reproductive and recruitment patterns in warthog population. Mammalia 32:6–29CrossRefGoogle Scholar
  14. Clutton-Brock TH, Guinnes FE, Albon S (1982) Red deer. Behaviour and ecology of two sexes. University of Chicago Press, ChicagoGoogle Scholar
  15. Clutton-Brock TH, Albon SD, Guiness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262. doi:10.1038/337260a0 CrossRefPubMedGoogle Scholar
  16. Cook RC, Murray DL, Cook JG, Zager P, Monfort SL (2001) Nutritional influences on breeding dynamics in elk. Can J Zool 79:845–853. doi:10.1139/cjz-79-5-845 CrossRefGoogle Scholar
  17. Côté SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238. doi:10.1007/s004420000584 CrossRefGoogle Scholar
  18. David JHM (1975) Observations on mating behaviour, parturition, suckling and the mother-young bond in bontebok (Damaliscus dorcas dorcas). J Zool 177:203–223CrossRefGoogle Scholar
  19. Desmukh IK (1984) A common relationship between precipitation and grassland peak biomass for east and southern Africa. Afr J Ecol 22:181–186. doi:10.1111/j.1365-2028.1984.tb00693.x CrossRefGoogle Scholar
  20. Du Plessis SS (1972) Ecology of blesbok with special reference to productivity. Wildlife Monograph 30. The Wildlife Society, Washington, D.C.Google Scholar
  21. Estes RD (1976) The significance of breeding synchrony in the wildebeest. Afr Wildl J 14:135–152Google Scholar
  22. Estes RD, Estes RK (1979) The birth and survival of wildebeest calves. Z Tierpsychol 50:54–95Google Scholar
  23. Fairall N (1968) The reproductive seasons of some mammals in the Kruger National Park. Zool Afr 3:189–210Google Scholar
  24. Festa-Bianchet M (1988) Birth date and survival in bighorn lambs (Ovis candensis). J Zool (Lond) 214:653–661. doi:10.1111/j.1469-7998.1988.tb03764.x CrossRefGoogle Scholar
  25. Gaillard J-M, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63. doi:10.1016/S0169-5347(97)01237-8 CrossRefGoogle Scholar
  26. Gaillard J-M, Festa-Bianchet M, Yoccoz NG, Loison A, Toigo C (2000) Temporal variation in fitness components and dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393. doi:10.1146/annurev.ecolsys.31.1.367 CrossRefGoogle Scholar
  27. Game Department Annual Reports (GDAR) (1954) Kenya Government Printers, Nairobi, KenyaGoogle Scholar
  28. Game Department Annual Reports (GDAR) (1962) Kenya Government Printers, Nairobi, KenyaGoogle Scholar
  29. Green WCH, Rothstein A (1993) Asynchronous parturition in bison: implications for the hider-follower dichotomy. J Mammal 74:920–925. doi:10.2307/1382430 CrossRefGoogle Scholar
  30. Grimsdell JJR (1973) Reproduction in the African buffalo, Syncerus caffer, in Western Uganda. J Reprod Fertil Suppl 19:303–318PubMedGoogle Scholar
  31. Hart GH, Guilbert HR (1933) Vitamin-A deficiency as related to reproduction in range cattle. Univ Calif Afr Exp Stat Bull 560Google Scholar
  32. Hastenrath S, Polzin D, Mutai C (2007) Diagnosing the 2005 drought in equatorial east Africa. J Clim 20:4628–4637. doi:10.1175/JCLI4238.1 CrossRefGoogle Scholar
  33. Hillman JC, Hillman AKK (1977) Mortality of wildlife in Nairobi National Park, during the drought of 1973–1974. Afr Wildl J 15:1–18Google Scholar
  34. Holland Ø, Mysterud A, Røed KH, Coulson T, Gjøstein H, Weladji RB, Nieminen M (2006) Adaptive adjustment of offspring sex ratio and maternal reproductive effort in an iteroparous mammal. Proc R Soc Lond B 273:293–299. doi:10.1098/rspb.2005.3330 CrossRefGoogle Scholar
  35. Howell CE, Rollins WC (1951) Environmental sources of variation in the gestation length of the horse. J Anim Sci 10:789–796Google Scholar
  36. Hulme M, Doherty R, Ngara T, New M, Lister D (2001) African climate change: 1900–2100. Clim Res 17:145–168. doi:10.3354/cr017145 CrossRefGoogle Scholar
  37. Hutchinson HG, MacFarlane JS (1958) Variation in gestation period of Zebu cattle under ranch conditions. Afr Agric For J 24:148–152Google Scholar
  38. Ims RA (1990a) The ecology and evolution of reproductive synchrony. Trends Ecol Evol 5:135–140. doi:10.1016/0169-5347(90)90218-3 CrossRefGoogle Scholar
  39. Ims RA (1990b) On the adaptive value of reproductive synchrony as a predator-swamping strategy. Am Nat 136:485–498. doi:10.1086/285109 CrossRefGoogle Scholar
  40. Kendall M, Stuart A (1979) Advanced theory of statistics. Inference and relationship, vol 2, 4th edn. Charles Griffin, LondonGoogle Scholar
  41. Kiltie RA (1982) Intraspecific variation in the mammalian gestation period. J Mammal 63:646–652. doi:10.2307/1380270 CrossRefGoogle Scholar
  42. Kitchen DW (1974) Social behaviour and ecology of pronghorn. Wildlife Monograph 38. The Wildlife Society, Washington, D.C.Google Scholar
  43. Langvatn R, Mysterud A, Stenseth NC, Yoccoz NG (2004) Timing and synchrony of ovulation in red deer constrained by short northern winters. Am Nat 163:763–772. doi:10.1086/383594 CrossRefPubMedGoogle Scholar
  44. Leuthold W, Leuthold BM (1975) Temporal patterns of reproduction in ungulates of Tsavo East National Park, Kenya. Afr Wildl J 13:159–169Google Scholar
  45. Linnell JDC, Andersen R (1998) Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus. J Zool (Lond) 244:497–504. doi:10.1111/j.1469-7998.1998.tb00055.x CrossRefGoogle Scholar
  46. Mason DR (1986) Reproduction in the male warthog Phacochoerus aethiopicus from Zululand, South Africa. S Afr J Zool 21:39–47Google Scholar
  47. McHugh MJ (2006) Impact of south pacific circulation variability on East African rainfall. Int J Climatol 26:505–521. doi:10.1002/joc.1257 CrossRefGoogle Scholar
  48. Mduma SAR, Sinclair ARE, Hilborn R (1999) Food regulates the Serengeti wildebeest: a 40-year record. J Anim Ecol 68:1101–1122. doi:10.1046/j.1365-2656.1999.00352.x CrossRefGoogle Scholar
  49. Millar JS (1977) Adaptive features of mammalian reproduction. Evol Int J Org Evol 31:370–386. doi:10.2307/2407759 Google Scholar
  50. Miller RF, Hart GH, Cole HG (1942) Fertility in sheep as affected by nutrition during breeding season and pregnancy. Univ Calif Afr Exp Stat Bull 672Google Scholar
  51. Mitchell B, Lincoln GA (1973) Conception dates in relation to age and condition in two populations of Red deer in Scotland. J Zool 171:141–152CrossRefGoogle Scholar
  52. Moe SR, Rutina LP, du Toit JT (2007) Trade-off between resource seasonality and predation risk explains reproductive chronology in impala. J Zool (Lond) 273:237–243. doi:10.1111/j.1469-7998.2007.00319.x CrossRefGoogle Scholar
  53. Nicholson SE, Entekhabi D (1986) The quasi-periodic behaviour of rainfall variability in Africa and its relationship to the Southern Oscillation. Arch Meteorol Geophys Bioclim Ser A 34:311–348. doi:10.1007/BF02257765 CrossRefGoogle Scholar
  54. Norton-Griffiths M, Herlocker DJ, Pennycuick L (1975) The patterns of rainfall in the Serengeti ecosystem. Afr Wildl J 13:347–374Google Scholar
  55. Oftedal OT (1984) Pregnancy and lactation. In: Hudson RJ, White RG (eds) Bioenergetics of wild herbivores. CRC Press, Boca Raton, FL, pp 215–238Google Scholar
  56. Ogutu JO, Piepho H-P, Dublin HT, Bhola N, Reid RS (2007) El Niño-Southern Oscillation, rainfall, temperature and Normalized Difference Vegetation Index fluctuations in the Mara-Serengeti ecosystem. Afr J Ecol 46:132–143. doi:10.1111/j.1365-2028.2007.00821.x CrossRefGoogle Scholar
  57. Ogutu JO, Piepho H-P, Dublin HT, Bhola N, Reid RS (2008) Rainfall influences on ungulate population abundance in the Mara-Serengeti ecosystem. J Anim Ecol 77:814–829. doi:10.1111/j.1365-2656.2008.01392.x CrossRefPubMedGoogle Scholar
  58. Piepho HP, Ogutu JO (2007) Simple state-space models in a mixed model framework. Am Stat 61:224–232. doi:10.1198/000313007X220426 CrossRefGoogle Scholar
  59. Post E (2004) Timing of reproduction in large mammals. In: Schwartz MD (ed) Phenology, an integrative environmental science. Springer, New York, pp 437–449Google Scholar
  60. Post E, Bøving PS, Perdersen C, MacArthur MA (2003) Synchrony between caribou calving and plant phenology in depredated and non-depredated populations. Can J Zool 81:1709–1714. doi:10.1139/z03-172 CrossRefGoogle Scholar
  61. Rachlow JL, Bowyer RT (1991) Interannual variation in timing and synchrony of parturition in Dall’s sheep. J Mammal 72:487–492. doi:10.2307/1382131 CrossRefGoogle Scholar
  62. Rodgers WA (1984) Warthog ecology in South east Tanzania. Mammalia 48:327–350CrossRefGoogle Scholar
  63. Russell DE, Gerhart KL, White RG, Van De Wetering DV (1998) Detection of early pregnancy in caribou: evidence for embryonic mortality. J Wildl Manag 62:1066–1075. doi:10.2307/3802559 CrossRefGoogle Scholar
  64. Rutberg AT (1984) Birth synchrony in American Bison (Bison bison): response to predation or season. J Mammal 65:418–423. doi:10.2307/1381088 CrossRefGoogle Scholar
  65. Rutberg AT (1987) Adaptive hypotheses of birth synchrony in ruminants: an interspecific test. Am Nat 130:692–710. doi:10.1086/284739 CrossRefGoogle Scholar
  66. Rutherford MC (1980) Annual plant production–precipitation relations in arid and semi-arid regions. S Afr J Sci 76:53–56Google Scholar
  67. Ryan SJ, Knechtel CV, Getz WM (2007) Ecological cues, gestation length, and birth timing in African buffalo (Syncerus caffer). Behav Ecol 18:635–644. doi:10.1093/beheco/arm028 CrossRefGoogle Scholar
  68. Sadleir RMFS (1969) The ecology of reproduction in wild and domesticated mammals. Methuen, LondonGoogle Scholar
  69. Saji NS, Goswami BN, Vinayachandran PN, Yamagata T (1999) A dipole mode in the tropical Indian Ocean. Nature 401:360–363PubMedGoogle Scholar
  70. SAS Institute (2005) SAS system for windows, version 9.1.3. SAS Institute Inc., CaryGoogle Scholar
  71. Sinclair ARE (1995) Population limitation of resident herbivores. In: Sinclair ARE, Arcese P (eds) Serengeti II. Dynamics, management and conservation of an ecosystem. University of Chicago Press, Chicago, pp 194–219Google Scholar
  72. Sinclair ARE, Mduma SAR, Arcese P (2000) What determines phenology and synchrony of ungulate breeding in Serengeti? Ecology 81:2100–2111CrossRefGoogle Scholar
  73. Taber RD, Dassmann RF (1958) The black-tailed deer of the chaparral. Calif. Dept. Fish and Game. Game Bulletin No. 8Google Scholar
  74. Talbot LM, Talbot MH (1963) The wildebeest in Western Maasialand, East AfricaWildlife Monograph 12. The Wildlife Society, Washington, D.C.Google Scholar
  75. Teer JG, Thomas JW, Walker EA (1965) Ecology and management of white-tailed deer in Llano Basin of Texas. Wildlife Monograph 15. The Wildlife Society, Washington, D.C.Google Scholar
  76. Testa JW (2002) Does predation on neonates inherently select for earlier births? J Mammal 83:699–706. doi:10.1644/1545-1542(2002)083<0699:DPONIS>2.0.CO;2 CrossRefGoogle Scholar
  77. Testa JW, Adams GP (1998) Body condition and adjustments to reproductive effort in female moose (Alces alces). J Mammal 79:1345–1354. doi:10.2307/1383026 CrossRefGoogle Scholar
  78. Thomson AM, Thomson W (1949) Lambing in relation to diet of the pregnant ewe. Br J Nutr 2:290–305. doi:10.1079/BJN19480056 CrossRefPubMedGoogle Scholar
  79. Verme LJ (1965) Reproduction studies on white-tailed deer. J Wildl Manage 29:74–79. doi:10.2307/3798633 CrossRefGoogle Scholar
  80. Watson RM (1969) Reproduction of wildebeest, Connochetes taurinus albojubatus Thomas, in the Serengeti region, and its significance to conservation. J Reprod Fertil Suppl 6:287–310Google Scholar
  81. Webster PJ, Moore AM, Loschnigg JP, Leben RR (1999) Coupled ocean-atmosphere dynamics in the Indian Ocean during 1997–1998. Nature 401:356–360. doi:10.1038/43848 CrossRefPubMedGoogle Scholar
  82. Wittemyer G, Rasmussen HB, Douglas-Hamilton I (2007) Breeding phenology in relation to NDVI variability in free-ranging African elephant. Ecography 30:42–50Google Scholar

Copyright information

© The Society of Population Ecology and Springer 2009

Authors and Affiliations

  • Joseph O. Ogutu
    • 1
    • 2
  • Hans-Peter Piepho
    • 2
  • Holly T. Dublin
    • 3
  • Nina Bhola
    • 4
  • Robin S. Reid
    • 1
  1. 1.International Livestock Research Institute (ILRI)NairobiKenya
  2. 2.Institut fuer Pflanzenbau und GruenlandUniversitaet HohenheimStuttgartGermany
  3. 3.Centre for Biodiversity Conservation, c/o South African National Biodiversity InstituteSpecies Survival Commission (SSC), The World Conservation Union (IUCN)Cape TownRepublic of South Africa
  4. 4.University of GroningenHarenThe Netherlands

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