Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Social rank and reproductive performance in a herd of farmed red deer females (Cervus elaphus)

M. Villagrán A C , L. Alvarez B and R. Ungerfeld A
+ Author Affiliations
- Author Affiliations

A Departamento de Fisiología, Facultad de Veterinaria, Universidad de la República, Uruguay.

B Centro de Enseñanza, Investigación y Extensión en Producción Animal en Altiplano, Universidad Nacional Autónoma de México, México.

C Corresponding author. Email: matiasv06@gmail.com

Animal Production Science - https://doi.org/10.1071/AN16838
Submitted: 18 May 2016  Accepted: 22 January 2017   Published online: 15 March 2017

Abstract

Hierarchical relationships between individuals determine unequal access to recourses like food and individuals of the other gender, resulting in a higher reproductive success of high-social ranked individuals. Environmental conditions and food availability may determine how strong these effects are. The aim of this work was to determine if social rank of farmed red deer females affect the reproductive results of a hormonal oestrous synchronisation treatment with ad libitum food. The studied responses included the time to oestrus onset, percentage of females that came into oestrus, conception and calving rates, gestation length, and calf gender. The study was performed during autumn on a research farm located in Mexico (20°36ʹ N, 99°55ʹ W). Forty-nine adult red deer females were assigned to two replications of 21 and 28 animals respectively and were allocated into independent paddocks with ad libitum food and water availability. Oestrous cycles were synchronised with a traditional protocol of intravaginal devices impregnated with progesterone. Agonistic behaviours between females were recorded (total = 1626 interactions), hierarchical position (Success Index = SI) of each animal was calculated and individuals were categorised as high (n = 13), medium (n = 20) or low-ranked (n = 16) individuals. Reproductive data were recorded during the 5 days after the oestrous synchronisation treatment and during the calving period. Any of the recorded responses differ between HR, MR and LR females. Female SI, age and bodyweight were not related with the probability of coming into oestrus, result pregnant, and giving birth to a male calf. Thirty-seven (78.5%) females of this study gave birth. From these calves, 15 were males and 22 were females. Due to high percentage of females in oestrus that gave birth (85.7%), it was not possible to detect the relationship between female SI, age, and bodyweight with the conception rate. Female SI, age and bodyweight were unrelated to time to oestrus onset (r2 = 0.09; P = 0.17), and to gestation length (r2 = 0.10; P = 0.20). In conclusion, with ad libitum high quality food, the social rank of red deer hinds did not affect the time to oestrus onset, percentage of females that came into oestrus, gestation length, calving and conception rates, and offspring sex ratio after an oestrous synchronisation hormonal treatment.

Additional keywords: cervid, dominance, offspring investment, sex ratio.


References

Altmann M, Altmann J (1991) Models of status-correlated bias in offspring sex ratio. American Naturalist 137, 542–555.
Models of status-correlated bias in offspring sex ratio.CrossRef |

Alvarez L, Martin G, Galindo F, Zarco L (2003) Social dominance of female goats affects their response to the male effect. Applied Animal Behaviour Science 84, 119–126.
Social dominance of female goats affects their response to the male effect.CrossRef |

Alvarez L, Zarco L, Galindo F, Blache D, Martin GB (2007) Social rank and response to the ‘male effect’ in the Australian Cashmere goat. Animal Reproduction Science 102, 258–266.
Social rank and response to the ‘male effect’ in the Australian Cashmere goat.CrossRef | 1:STN:280:DC%2BD2snitFOmtw%3D%3D&md5=3275bfdb1c8fb1c938d8512c8ca5924aCAS |

Appleby MC (1980) Social rank and food access in red deer stags. Behaviour 74, 294–309.
Social rank and food access in red deer stags.CrossRef |

Asher GW (2007) Gestation length in red deer: genetically determined or environmentally controlled? In ‘Reproduction in domestic ruminants VI’. (Eds JL Juengel, JF Murray, MF Smith) pp. 255–260. (Nottingham University Press: Nottingham)

Barroso FG, Alados CL, Boza J (2000) Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science 69, 35–53.
Social hierarchy in the domestic goat: effect on food habits and production.CrossRef | 1:STN:280:DC%2BC2sbitlOmuw%3D%3D&md5=01343241c69e4420a66cd180b6efe348CAS |

Bartoš L, Schams D, Bubenik G, Kotrba R, Tománek M (2010) Relationship between rank and plasma testosterone and cortisol in red deer males (Cervus elaphus). Physiology & Behavior 101, 628–634.
Relationship between rank and plasma testosterone and cortisol in red deer males (Cervus elaphus).CrossRef |

Bro-Jørgensen J (2002) Overt female mate competition and preference for central males in a lekking antelope. Proceedings of the National Academy of Sciences of the United States of America 99, 9290–9293.
Overt female mate competition and preference for central males in a lekking antelope.CrossRef |

Bro-Jørgensen J (2011) Intra- and intersexual conflicts and cooperation in the evolution of mating strategies: lessons learnt from ungulates. Evolutionary Biology 38, 28–41.
Intra- and intersexual conflicts and cooperation in the evolution of mating strategies: lessons learnt from ungulates.CrossRef |

Cameron EZ, Linklater WL (2007) Extreme sex ratio variation in relation to change in condition around conception. Biology Letters 3, 395–397.
Extreme sex ratio variation in relation to change in condition around conception.CrossRef |

Cassinello J (1996) High-ranking females bias their investment in favour of male calves in captive Ammotragus lervia. Behavioral Ecology and Sociobiology 38, 417–424.
High-ranking females bias their investment in favour of male calves in captive Ammotragus lervia.CrossRef |

Cassinello J, Gomendio M (1996) Adaptive variation in litter size and sex ratio at birth in a sexually dimorphic ungulate. Proceedings of the Royal Society of London. Series B, Biological Sciences 263, 1461–1466.
Adaptive variation in litter size and sex ratio at birth in a sexually dimorphic ungulate.CrossRef |

Ceacero F, García AJ, Landete-Castillejos T, Bartošová J, Bartoš L, Gallego L (2012) Benefits for dominant red deer hinds under a competitive feeding system: food access behavior, diet and nutrient selection. PLoS One 7, e32780
Benefits for dominant red deer hinds under a competitive feeding system: food access behavior, diet and nutrient selection.CrossRef | 1:CAS:528:DC%2BC38XjvFaju7g%3D&md5=8628a6ad5b267776292f0575f37452b2CAS |

Chunwang L, Zhigang J, Yan Z, Caie Y (2004) Relationship between serum testosterone, dominance and mating success in Père David’s deer stags. Ethology 110, 681–691.
Relationship between serum testosterone, dominance and mating success in Père David’s deer stags.CrossRef |

Clements MN, Clutton-Brock TH, Albon SD, Pemberton JM, Kruuk LEB (2011) Gestation length in wild ungulates. Functional Ecology 25, 691–703.
Gestation length in wild ungulates.CrossRef |

Clutton-Brock TH, Huchard E (2013) Social competition and its consequences in female mammals. Journal of Zoology 289, 151–171.
Social competition and its consequences in female mammals.CrossRef |

Clutton-Brock TH, Guinness FE, Albon SD (1982) ‘Red deer behavior and ecology of two sexes.’ (Ed. GB Schaller) (University of Chicago Press: Chicago)

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

Clutton-Brock TH, Albon SD, Guinness FE (1986) Great expectations: dominance, breeding success and offspring ratios in red deer. Animal Behaviour 34, 460–471.
Great expectations: dominance, breeding success and offspring ratios in red deer.CrossRef |

Côté SD (2000) Dominance hierarchies in female mountain goats: stability, aggressiveness and determinants of rank. Behaviour 137, 1541–1566.
Dominance hierarchies in female mountain goats: stability, aggressiveness and determinants of rank.CrossRef |

Côté SD, Festa Bianchet M (2001) Reproductive success in female mountain goats: the influence of age and social rank. Animal Behaviour 62, 173–181.
Reproductive success in female mountain goats: the influence of age and social rank.CrossRef |

Dušek A, Bartoš L, Švecová L (2007) The effect of a mother’s rank on her offspring’s pre-weaning rank in farmed red deer. Applied Animal Behaviour Science 103, 146–155.
The effect of a mother’s rank on her offspring’s pre-weaning rank in farmed red deer.CrossRef |

Endo A, Doi T, Shiraki A (1997) Post-copulative guarding: mating behaviour of non-territorial male sika deer (Cervus nippon) in an enclosure. Applied Animal Behaviour Science 54, 257–263.
Post-copulative guarding: mating behaviour of non-territorial male sika deer (Cervus nippon) in an enclosure.CrossRef |

Favre M, Martin JGA, Festa-Bianchet M (2008) Determinants and life-history consequences of social dominance in bighorn ewes. Animal Behaviour 76, 1373–1380.
Determinants and life-history consequences of social dominance in bighorn ewes.CrossRef |

Fiol C, Ungerfeld R (2011) Males’ sexual preference toward heavier heifers is only observed in competitive situations with lighter heifers. Livestock Science 139, 281–284.
Males’ sexual preference toward heavier heifers is only observed in competitive situations with lighter heifers.CrossRef |

Gomendio M, Clutton-Brock TH, Albon SD, Guinness FE, Simpson MJ (1990) Mammalian sex ratios and variation in costs of rearing sons and daughters. Nature 343, 261–263.
Mammalian sex ratios and variation in costs of rearing sons and daughters.CrossRef | 1:STN:280:DyaK3c7js1yqtQ%3D%3D&md5=2aa066fc344e72f5d42b80dd0f6ff642CAS |

Guinness FE, Clutton-Brock TH, Albon SD (1978) Factors affecting calf mortality in red deer (Cervus elaphus). Journal of Animal Ecology 47, 817–832.
Factors affecting calf mortality in red deer (Cervus elaphus).CrossRef |

Hirotani A (1994) Dominance rank, copulatory behaviour and estimated reproductive success in male reindeer. Animal Behaviour 48, 929–936.
Dominance rank, copulatory behaviour and estimated reproductive success in male reindeer.CrossRef |

Hohenbrink S, Meinecke-Tillmann S (2012) Influence of social dominance on the secondary sex ratio and factors affecting hierarchy in Holstein dairy cows. Journal of Dairy Science 95, 5694–5701.
Influence of social dominance on the secondary sex ratio and factors affecting hierarchy in Holstein dairy cows.CrossRef | 1:CAS:528:DC%2BC38XhsVCnsLzL&md5=a7b0004e93c00a33eabf7f71272ce17fCAS |

Holand Ø, Weladji RB, Gjøstein H, Kumpula J, Smith ME, Nieminen M, Røed KH (2004) Reproductive effort in relation to maternal social rank in reindeer (Rangifer tarandus). Behavioral Ecology and Sociobiology 57, 69–76.
Reproductive effort in relation to maternal social rank in reindeer (Rangifer tarandus).CrossRef |

Hurnik JF, Lewis NJ, Taylor A, Pinheiro Machado LC (1995) Social hierarchy. In ‘Farm animal behaviour. Laboratory manual’. (Eds JF Hurnik, NJ Lewis, A Taylor, LC Pinheiro Machado) pp. 79–89. (University of Guelph: Guelph)

Ingrand S (2000) Feeding behaviour, intake and performance in beef cattle managed in groups. Productions Animales 13, 151–163.

Jørgensen GHM, Andersen IL, Bøe KE (2007) Feed intake and social interactions in dairy goats – The effects of feeding space and type of roughage. Applied Animal Behaviour Science 107, 239–251.
Feed intake and social interactions in dairy goats – The effects of feeding space and type of roughage.CrossRef |

Kidjo N, Serrano E, Bideau E, Gonzalez G (2016) Is dominance the only factor determining access to food in an agonistic context? An experiment with captive male mouflon. Acta Ethologica 19, 69–79.
Is dominance the only factor determining access to food in an agonistic context? An experiment with captive male mouflon.CrossRef |

Kojola I (1997) Social status and physical condition of mother and sex ratio of offspring in cervids. Applied Animal Behaviour Science 51, 267–274.
Social status and physical condition of mother and sex ratio of offspring in cervids.CrossRef |

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.
Population density affects sex ratio variation in red deer.CrossRef | 1:CAS:528:DyaK1MXjvV2jt7Y%3D&md5=1ad2266a76ee728bb32a7dabadc768a0CAS |

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). Behavioral Ecology and Sociobiology 57, 267–274.
Maternal quality and differences in milk production and composition for male and female Iberian red deer calves (Cervus elaphus hispanicus).CrossRef |

Luna-Estrada AA, Vera-Avila HR, Mora O, Anguiano-Serrano B, Vazquez-Pelaez CG, Shimada A (2006) Effect of pre-mating nutritional status in red deer (Cervus elaphus scoticus) hinds on the sex ratio of their offspring. Small Ruminant Research 65, 154–160.
Effect of pre-mating nutritional status in red deer (Cervus elaphus scoticus) hinds on the sex ratio of their offspring.CrossRef |

Matsuzawa Y, Hagiya K (1991) Relationship between feeding behavior and social dominance in a small herd of goats. Scientific Reports of the Faculty of Agriculture, Ibaraki University 39, 1–6.

McElligott AG, Gammell MP, Harty HC, Paini DR, Murphy DT, Walsh JT, Hayden TJ (2001) Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success? Behavioral Ecology and Sociobiology 49, 266–272.
Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success?CrossRef |

Miranda-de la Lama GC, Sepúlveda WS, Montaldo HM, María GA, Galindo F (2011) Social strategies associated with identity profiles in dairy goats. Applied Animal Behaviour Science 134, 48–55.
Social strategies associated with identity profiles in dairy goats.CrossRef |

Morales-Piñeyrúa JT, Ciappesoni G, Ungerfeld R (2014) Social rank and reproductive performance of pampas deer females (Ozotoceros bezoarticus, Linnaeus, 1758). Behavioural Processes 105, 49–52.
Social rank and reproductive performance of pampas deer females (Ozotoceros bezoarticus, Linnaeus, 1758).CrossRef |

Ozoga JJ (1972) Aggressive behavior of White-tailed deer at winter cuttings. The Journal of Wildlife Management 36, 861–868.
Aggressive behavior of White-tailed deer at winter cuttings.CrossRef |

Pascual-Alonso M, María GA, Sepúlveda WS, Villarroel M, Aguayo-Ulloa L, Galindo F, Miranda-de la Lama GC (2013) Identity profiles based on social strategies, morphology, physiology, and cognitive abilities in goats. Journal of Veterinary Behavior 8, 458–465.
Identity profiles based on social strategies, morphology, physiology, and cognitive abilities in goats.CrossRef |

Plard F, Gaillard JM, Coulson T, Hewison AJM, Douhard M, Klein F, Delorme D, Warnant C, Bonenfant C (2015) The influence of birth date via body mass on individual fitness in a long-lived mammal. Ecology 96, 1516–1528.
The influence of birth date via body mass on individual fitness in a long-lived mammal.CrossRef |

Price EO (1999) Behavioral development in animals undergoing domestication. Applied Animal Behaviour Science 65, 245–271.
Behavioral development in animals undergoing domestication.CrossRef |

Rosenfeld CS, Roberts RM (2004) Maternal diet and other factors affecting offspring sex ratio: a review. Biology of Reproduction 71, 1063–1070.
Maternal diet and other factors affecting offspring sex ratio: a review.CrossRef | 1:CAS:528:DC%2BD2cXnvVGqtrY%3D&md5=702e8f77b04ec5aada2108025181b308CAS |

Šárová R, Špinka M, Stěhulová I, Ceacero F, Šimečková M, Kotrba R (2013) Pay respect to the elders: Age, more than body mass, determines dominance in female beef cattle. Animal Behaviour 86, 1315–1323.
Pay respect to the elders: Age, more than body mass, determines dominance in female beef cattle.CrossRef |

Shargal D, Shore L, Roteri N, Terkel A, Zorovsky Y, Shemesh M, Steinberger Y (2008) Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring. Theriogenology 69, 673–680.
Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring.CrossRef | 1:CAS:528:DC%2BD1cXjtVWhs7Y%3D&md5=a6bdc91473a82a5b7a972b71b205a8feCAS |

Sherwin CM, Johnson KG (1987) The influence of social factors on the use of shade by sheep. Applied Animal Behaviour Science 18, 143–155.
The influence of social factors on the use of shade by sheep.CrossRef |

Shipka MP, Rowell JE (2010) Gestation length in farmed reindeer. In ‘Reproduction in domestic ruminants’. (Eds MC Lucy, JL Pate, MF Smith, TE Spencer) pp. 457–466. (Nottingham University Press: Nottingham)

Silk JB (1983) Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. American Naturalist 121, 56–66.
Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities.CrossRef |

Stockley P, Bro-Jørgensen J (2011) Female competition and its evolutionary consequences in mammals. Biological Reviews of the Cambridge Philosophical Society 86, 341–366.
Female competition and its evolutionary consequences in mammals.CrossRef |

Taillon J, Côté SD (2007) Social rank and winter forage quality affect aggressiveness in white-tailed deer fawns. Animal Behaviour 74, 265–275.
Social rank and winter forage quality affect aggressiveness in white-tailed deer fawns.CrossRef |

Thouless CR (1990) Feeding competition between grazing red deer hinds. Animal Behaviour 40, 105–111.
Feeding competition between grazing red deer hinds.CrossRef |

Thouless CR, Guinness FE (1986) Conflict between red deer hinds: the winner always wins. Animal Behaviour 34, 1166–1171.
Conflict between red deer hinds: the winner always wins.CrossRef |

Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92.
Natural selection of parental ability to vary the sex ratio of offspring.CrossRef | 1:STN:280:DyaE3s%2Fls1Wqsg%3D%3D&md5=d0f7975832b9b29eb64ffe65c572f79bCAS |

Ungerfeld R, Correa O (2007) Social dominance of female dairy goats influences the dynamics of gastrointestinal parasite eggs. Applied Animal Behaviour Science 105, 249–253.
Social dominance of female dairy goats influences the dynamics of gastrointestinal parasite eggs.CrossRef |

Ungerfeld R, González-Pensado SP (2008) Social rank affects reproductive development in male lambs. Animal Reproduction Science 109, 161–171.
Social rank affects reproductive development in male lambs.CrossRef | 1:STN:280:DC%2BD1cnpt1CltQ%3D%3D&md5=339d6a26fbd39a2a0444e75ccf3da568CAS |

Ungerfeld R, González-Pensado S, Dago AL, Vilariño M, Menchaca A (2007) Social dominance of female dairy goats and response to oestrous synchronisation and superovulatory treatments. Applied Animal Behaviour Science 105, 115–121.
Social dominance of female dairy goats and response to oestrous synchronisation and superovulatory treatments.CrossRef |

Ungerfeld R, Cajarville C, Rosas MI, Repetto JL (2014) Time budget differences of high-and low-social rank grazing dairy cows. New Zealand Journal of Agricultural Research 57, 122–127.
Time budget differences of high-and low-social rank grazing dairy cows.CrossRef |

Vander Wal E, Yip H, McLoughlin PD (2012) Sex-based differences in density-dependent sociality: an experiment with a gregarious ungulate. Ecology 93, 206–212.
Sex-based differences in density-dependent sociality: an experiment with a gregarious ungulate.CrossRef | 1:STN:280:DC%2BC38rjtlGitQ%3D%3D&md5=624c1a97f34b0fcd700e81044c0e027eCAS |

Veiberg V, Loe LE, Mysterud A, Langvatn R, Stensenth NC (2004) Social rank, feeding and winter weight loss in red deer: any evidence of interference competition? Oecologia 138, 135–142.
Social rank, feeding and winter weight loss in red deer: any evidence of interference competition?CrossRef |



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