Skip to main content

Advertisement

Log in

ENSO affects sex ratio progeny in captive Iberian red deer despite a steady feeding regime

  • Original Paper
  • Published:
Acta Theriologica Aims and scope Submit manuscript

Abstract

Climate variability greatly affects animals through direct and indirect effects. Animals with slow reproductive adaptation to ecological changes such as large mammals are likely to have evolved mechanisms to anticipate early such impacts of climate variability on the environment. One of the adaptive mechanisms between reproductive costs and benefits in mammals affects parental investment through biases in sex ratio. Deer might be likely to show an early detection of climate variability because conception takes place in early autumn, but the main raising cost in deer concerns lactation, which takes place at the end of the following spring. The aim of this paper is to assess whether there is a relationship between global indices of climate variability such as El Niño-Southern Oscillation (ENSO) and sex ratio of a captive population of deer. Results showed that there was a negative correlation (r=−0.65) between sex ratio and ENSO indices between 1996 and 2008. El Niño enhances drier conditions during the summer in the Iberia Peninsula, which in turn favours a female bias. Results also suggest that the mechanism of early detection of climate variability exerts a strong effect on female reproductive physiology because the long-term stability of food resources in our setting has not markedly reduced it.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467–484

    Article  PubMed  Google Scholar 

  • Arnbom T, Fedak MA, Rothery P (1994) Offspring sex ratio in relation to female size in southern elephant seals, Mirounga leonina. Behav Ecol Sociobiol 35:373–378

    Article  Google Scholar 

  • ASAB (2006) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 71:245–253

    Article  Google Scholar 

  • Brelurut A, Pingard A, Thériez M (1990) Le cerf et son élevage. INRA, Paris, France

    Google Scholar 

  • Bugalho MN, Milne JA (2003) The composition of the diet of red deer (Cervus elaphus) in a Mediterranean environment: a case of summer nutritional constraint? For Ecol Manag 181:23–29

    Article  Google Scholar 

  • Carrion D, Garcia AJ, Gaspar-Lopez E, Landete-Castillejos T, Gallego L (2008) Development of body condition in hinds of Iberian red deer during gestation and its effects on calf birth weight and milk production. J Exp Zool 309A:1–10

    Article  Google Scholar 

  • Cassinello J (1996) High-ranking females bias their investment in favour of male calves in captive Ammotragus lervia. Behav Ecol Sociobiol 38:417–424

    Article  Google Scholar 

  • Chen D, Cane MA (2008) ENSO prediction and predictability. J Comput Phys 227:3625–3640

    Article  Google Scholar 

  • Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201:163–165

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH, Guinnes FE, Albon SD (1983) The costs of reproduction to red deer hinds. J Anim Ecol 52:367–383

    Article  Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1984) Maternal dominance, breeding success and birth sex-ratios in red deer. Nature 308:358–360

    Article  Google Scholar 

  • Clutton-Brock TH, Major M, Guinness FE (1985) Population regulation in male and female red deer. J Anim Ecol 54:831–846

    Article  Google Scholar 

  • Clutton-Brock TH, Iason GR (1986) Sex ratio variation in mammals. Q Rev Biol 61:339–374

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH (1991) Lords of the Lek—England fallow deer bucks create a common ground for attracting does. Natural History 34–41

  • Diaz P, Pedreira J, Sánchez-Andrade R, Suárez JL, Arias M, Francisco I, Fernández G, Díez-Baños P, Morrondo P, Paz-Silva A (2007) Risk periods of infection by Calicophoron daubneyi (Digenea: Paramphistomidae) in cattle from oceanic climate areas. Parasitol Res 101:339–342

    Article  PubMed  Google Scholar 

  • Dong B, Sutton RT, Scaife AA (2006) Multidecadal modulation of El Nino-Southern Oscillation (ENSO) variance by Atlantic Ocean sea surface temperatures. Geophys Res Lett. doi:10.1029/2006GL025766

  • Esteban-Parra MJ, Pozo-Vázquez D, Castro-Díez Y, Trigo RM (2004) Impacto de la NAO sobre las temperaturas máximas y mínimas de la Península Ibérica. XXVIII Jornadas Científicas de la AME. http://www.ame-web.org/jornadas_badajoz.htm Accessed 15 Nov 2008

  • Garcia AJ, Landete-Castillejos T, Garde JJ, Gallego L (2002) Reproductive seasonality in female Iberian red deer (Cervus elaphus hispanicus). Theriogenology 58:1553–1562

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Ispierto I, Lopez-Gatius F, Bech-Sabat G, Santolaria P, Yaniz JL, Nogareda C, De Rensis F, Lopez-Bejar M (2007) Climate factors affecting conception rate of high producing dairy cows in northeastern Spain. Theriogenology 67:1379–1385

    Article  CAS  PubMed  Google Scholar 

  • Garroway CJ, Broders HG (2005) The quantitative effects of population density and winter weather on the body condition of white-tailed deer (Odocoileus virginianus) in Nova Scotia, Canada. Can J Zool 83:1246–1256

    Article  Google Scholar 

  • Gouirand I, Moron V (2000) Intra-seasonal and multi-decadal variability of the ENSO/LNSO teleconnection with sea level pressure (100°W–50°E; 30°–70°N) between 1873 and 1996. Cr Acad Sci II A 331:633–640

    Google Scholar 

  • Green WCH, Rothstein A (1991) Trade-offs between growth and reproduction in female bison. Oecologia 86:521–527

    Article  PubMed  Google Scholar 

  • Kiladiz G, Diaz H (1989) Global climate anomalies associated with extremes in the Southern-Oscillation. J Climate 2:1069–1090

    Article  Google Scholar 

  • Kruuk LEB, Clutton-Brock TH, Albon SD, Pemberton JM, Guinness FE (1999) Population density affects sex ratio variation in red deer. Nature 399:459–461

    Article  CAS  PubMed  Google Scholar 

  • Landete-Castillejos T, Garcia A, Langton S, Inglis I, Gallego L, Garde J (2001) Opposing offspring sex ratio variations with increasing age and weight in mouflon mothers (Ovis musimon). Acta Vet Hung 49:257–268

    Article  CAS  PubMed  Google Scholar 

  • Landete-Castillejos T, García A, Gómez JA, Gallego L (2003) Lactation under food constraints in Iberian red deer Cervus elaphus hispanicus. Wildl Biol 9:131–139

    Google Scholar 

  • Landete-Castillejos T, Gortazar C, Vicente J, Fierro Y, García A, Gallego L (2004) Age-related foetal sex ratio bias in Iberian red deer (Cervus elaphus hispanicus): are male calves too expensive for growing mothers? Behav Ecol Sociobiol 56:1–8

    Article  Google Scholar 

  • Landete-Castillejos T, Garcia A, Lopez-Serrano FR, Gallego L (2005) Maternal quality and differences in milk production and composition for male and female Iberian red deer calves (Cervus elaphus hispanicus). Behav Ecol Sociobiol 57:267–274

    Article  Google Scholar 

  • Latif M, Anderson D, Barnett T, Cane M, Kleeman R, Leetmaa A, O'Brien J, Rosati A, Schneider E (1998) A review of the predictability and prediction of ENSO. J Geophys Res 103:14375–14393

    Article  Google Scholar 

  • Liu W, Wan X, Zhong W (2007) Population dynamics of the Mongolian gerbils: seasonal patterns and interactions among density, reproduction and climate. J Arid Environ 68:383–397

    Article  Google Scholar 

  • Muñoz-Díaz D, Rodrigo FS (2006) Seasonal rainfall variations in Spain (1912–2000) and their links to atmospheric circulation. Atmos Res 81:94–110

    Article  Google Scholar 

  • Mysterud A, Yoccoz NG, Stenseth NC, Langvatn R (2000) Relationships between sex ratio, climate and density in red deer: the importance of spatial scale. J Anim Ecol 69:959–974

    Article  Google Scholar 

  • Oftedal OT (1985) Pregnancy and lactation. Bioenergetics of wild herbivores. In: Hudson R, White RG (Eds.). CRC Press: 215–238

  • Pettorelli N, Mysterud A, Yoccoz NG, Langvatn R, Stenseth NC (2005) Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes. Proc Biol Sci 272:2357–2364

    Article  PubMed  PubMed Central  Google Scholar 

  • Plisnier PD, Serneels S, Lambin EF (2000) Impact of ENSO on East African ecosystems: a multivariate analysis based on climate and remote sensing data. Global Ecol Biogeogr 9:481–497

    Article  Google Scholar 

  • Post E, Forchhammer MC, Stenseth NC, Langvatn R (1999) Extrinsic modification of vertebrate sex ratios by climatic variation. Am Nat 154:194–204

    Article  PubMed  Google Scholar 

  • Silk JB (1983) Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. Am Nat 121:56–66

    Article  Google Scholar 

  • Stenseth NC, Ottersen G, Hurrell JW, Mysterud A, Lima M, Chan K-S, Yoccoz NG, Ådlandsvik B (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation. El Niño Southern Oscillation and beyond. Proc Biol Sci 270:2087–2096

    Article  PubMed  PubMed Central  Google Scholar 

  • Thouless CR, Guinness FE (1986) Conflict between red deer hinds—the winner always wins. Anim Behav 34:1166–1171

    Article  Google Scholar 

  • Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

    Article  CAS  PubMed  Google Scholar 

  • Van Oldenborgh GJ, Burgers G, Tank A (2000) On the El Niño teleconnection to spring precipitation in Europe. Int J Climatol 20:565–574

    Article  Google Scholar 

  • Vide JM, Fernández-Belmonte J (2001) El índice NAO y la precipitación mensual en la España Peninsular. Investig Geográficas 26:41–58

    Article  Google Scholar 

  • Wolter K, Timlin MS (1998) Measuring the strength of ENSO events—how does 1997/98 rank? Weather 53:315–324

    Article  Google Scholar 

  • Weladji RB, Klein DR, Holand Ø, Mysterud A (2002) Comparative response of Rangifer tarandus and other northern ungulates to climatic variability. Rangifer 22:29–46

    Google Scholar 

  • White TCR (2008) The role of food, weather and climate in limiting the abundance of animals. Biol Rev 83:227–248

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Fulgencio Cebrián and Isidoro Cambronero for their help in handling the animals. This study was supported by projects PAC06-01304298 (JCCM), MCYT (PET2006_0263), PBI 05–040 (JCCM), FEDER-MCEI project (CGL2008-00749/BOS) and MICINN (PTQ-08-01-06587). Handling procedures and sampling frequency were designed to reduce stress and health risks for subjects according to European and Spanish law, and current guidelines for ethical use of animals in research (ASAB 2006). We further thank the associate editor and three anonymous referees, for valuable comments on an earlier draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jose A. Estevez.

Additional information

Communicated by: Matt W. Hayward

Rights and permissions

Reprints and permissions

About this article

Cite this article

Estevez, J.A., Landete-Castillejos, T., García, A.J. et al. ENSO affects sex ratio progeny in captive Iberian red deer despite a steady feeding regime. Acta Theriol 56, 323–328 (2011). https://doi.org/10.1007/s13364-011-0036-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-011-0036-y

Keywords

Navigation