Epimeletic behaviour in farm animals: Evolution from wild ancestors through domestication to modern systems

Introduction

Epimeletic behaviour refers to care-giving actions expressed by one individual toward another, often directed to offspring, injured, or distressed conspecifics (Hafez & Bouissou, 2005). Animals perform et-epimeletic behaviours when they seek help from others through vocalizations and approach behaviour. The two elements serve as essential components which enable social species to maintain social cohesion and survive in their environments. Animals show epimeletic behaviour through their natural instinct to lick and groom as well as their actions of nursing, protecting and brooding their young ones. These behaviours developed through evolution to improve offspring survival rates and create stronger social bonds which maintained herd stability. They directly impact animal production and newborn survival and welfare outcomes in farm animals (Fraser & Broom, 2022) [16] . Domestication defined as the sustained multi-generational relationship between humans and animals where humans control breeding and living conditions has profoundly affected animal behaviour. Although domestication preserved many caregiving instincts, intensive management systems have increasingly constrained their expression (Price, 2002). The study of epimeletic behaviour evolution from wild ancestors to domestic animals requires this knowledge to develop welfare-friendly livestock management systems.

Domestication and Behavioural Evolution

The process of domestication started during the period from 11,000 to 3,000 years ago and resulted in behavioural and physiological and morphological transformations which scientists call the domestication syndrome. Early domesticated animals such as sheep and goats were initially managed in semi-natural conditions, allowing expression of full maternal and social behaviour. The process of selective breeding for docility and productivity and fast growth rates over thousands of years led to unintentional decreases in epimeletic responses among certain species. The ability to adapt behaviour proved essential for animals to become successfully domesticated. The selection process favoured animals which exhibited lower fear responses along with better social behaviour and ability to stay in confined spaces. The changes brought about modifications to maternal vigilance and protective aggression and allogrooming behaviour in the animals. [3] . The cow keeps the calf hidden at first for about a week and then gradually introduces it to the herd. After this period, calves form crèches; these are communal nurseries guarded and sometimes cared for by several adults in the herd. Wild aurochs, the ancestors of domestic cattle, displayed similar alloparental care. They collectively defended calves against predators and allowed motheroffspring bonds to form in a social setting. With domestication, these maternal behaviours initially continued under traditional pastoralism. However, the increase in intensive dairying led to a conflict between milk harvesting and maternal care. Modern dairy farms often separate calves from cows within hours of birth, frequently less than 24 hours, abruptly removing maternal contact. Studies show that this forced early separation causes intense distress vocalizations in both cows and calves and leads to abnormal searching behaviour (Johnsen et al., 2016) [20] . In contrast, cows allowed to stay in contact produce more affiliative calls and show fewer signs of stress. Beef cattle systems usually keep cow-calf contact for weeks (Fraser & Broom, 2022) [16] . Calves raised with their mothers tend to be calmer and show better thermoregulation and weight gains. While traditional herding maintained natural care patterns, modern systems, especially in dairy farming, have significantly reduced the duration and intensity of maternal care.

Sheep (Ovis aries)

In wild sheep, like the mouflon, ewes develop strong bonds with their lambs. Right after birth, the ewe licks and grooms each lamb while making soft bleats. This behaviour cleans and warms the lambs. It also helps the lambs recognize their mother's scent, creating a special memory. Lambs call out to find their mothers.

Goats (Capra hircus)

Goats, like sheep, inherit strong maternal behaviours from their wild ancestors, such as the Bezoar ibex. Around the time of giving birth, a doe seeks a hidden spot and gives birth in privacy. She immediately licks and sniffs her kid, marking it with her scent. Within hours, she forms a bond with her kid through recognizing its smell. Controlled studies of domestic goats show that mothers lick their newborns actively and quickly establish a bond through this scent recognition. Within four hours, they can recognize their offspring's appearance and sounds. Wild kids often stay hidden for their first week of life and join the herd only after they have suckled safely. Domesticated goats keep these instincts; small-scale herding systems let them stay with their kids for weeks. Only in intensive dairy systems are kids removed early, breaking the normal grooming and nursing process. In low-input or traditional systems, does still nurse, groom, and guide their kids much like wild does do, promoting strong social learning and survival. In modern farming, piglets are generally separated from their mothers after weaning. In traditional pastoral or smallholder settings, like with feral or free-range pigs, piglets typically stay in the nest for one to two weeks, nursing often, usually every 15 minutes, until weaning.

Pigs (Sus

Chickens (Gallus gallus domesticus)

The ancestor of the domestic chicken, the Red Junglefowl, shows full maternal care. A broody hen incubates her eggs in a nest, then cares for the newly hatched chicks. She leads them to food and shelter while warning them of danger. In natural broods, the mother and chicks stay closely bonded for 5 to 12 weeks. Even before hatching, embryo chicks make distress calls that prompt the hen to respond, helping the chicks recognize her voice after they hatch. Once chicks are hatched, a broody hen uses special calls to keep her family together: "food calls" and "cluck" calls gather chicks when it's time to eat, while alarm calls warn of predators. Chicks imprint on the mother's appearance and cluck calls during their first days of life. Domestication initially maintained this maternal behaviour, but selective breeding has changed it greatly. Commercial layers have been bred to reduce broodiness, so hens rarely build nests or raise chicks. In industrial flocks, eggs go into incubators, and the chicks do not receive maternal care. However, heritage and backyard hens still have these instincts. When given the chance, they will brood eggs and care for their chicks naturally. These observations show that the genetic potential for maternal care is still there, even if modern production systems usually suppress it.

Horses (Equus caballus)

Wild horses live in family groups with strong mare-foal bonds. Foals in this species are able to stand and nurse within the first hour of life. Mares and foals form immediate bonds. If a mare moves away, the foal follows her closely. If the foal lies down, the mare stands guard. Foals nurse frequently, often every 15 minutes during their first month, and mothers reject any alien foals. Mares groom their foals and show protective behaviour toward threats. For the first month, foals mainly interact with their mothers, starting to explore and play with other horses only later. Mares may nurse their offspring for a year or more if left undisturbed. Domestication has not eliminated these instincts. Foals of domestic mares still follow and nuzzle their mothers, and mutual grooming and social learning happen in pastured horses. However, human management often cuts short natural care. Most foals are weaned at 4 to 6 months, much earlier than the natural weaning age of 10 to 11 months, and are regularly handled by humans. Horses can form bonds with other adults and develop friendships, such as mutual grooming between mares, even in domestic settings. There are anecdotal reports of horses responding to distressed humans or forming bonds with other species, indicating their strong social instincts remain, but these events have mostly been noted by horse owners rather than through formal research.

Donkeys (Equus asinus)

Donkeys come from the African wild ass, and their maternal behaviour is similar to that of horses. Jennies give birth in front of the herd and quickly form a close bond with their foals. A recent study of Somali wild asses, which are closely related, found that foals continue to nurse until they are yearlings, around 10 to 12 months old. This suggests that mothers nurse for a long time in these animals. In domestic donkeys, mares stay close to their foals and groom them at first, gradually allowing more independence. Because donkeys are rarely farmed intensively, traditional care usually lets foals remain with their mothers for many months. Recent studies confirm that wild asses have prolonged nursing and stable mother-foal interactions, suggesting that donkey maternal care has stayed mostly the same despite domestication.

Camels (Camelus spp.)

The available literature did not provide detailed accounts of camel maternal behaviour, so we turn to general knowledge. Wild camelids, both dromedaries and Bactrians, establish strong bonds with their calves. Calves can walk and run shortly after birth and typically stay close to their mothers for many months, nursing for more than a year. Domestication, which began about 4,000 years ago, did not remove these instincts. In pastoral societies today, mother camels usually raise one calf at a time, with extended nursing and social bonding. Some modern dairy camel farms practice partial separation, like removing the calf at milking time to boost milk production. However, nomadic herders typically allow calves to suckle freely. Overall, camels keep their long maternal nursing periods and bonding behaviours, although we could not find a direct source that provides specific details on this species.

Conclusion

References

1. Alexander G. Maternal behaviour in the ewe and its influence on lamb survival. Journal of Animal Science. 1962;21(3):330-342. https://doi.org/10.2527/jas1962.213330x
2. Arey DS. Behavioural observations of peri-parturient sows and the development of alternative farrowing accommodation: A review. Animal Welfare. 1997;6(3):217-229.
3. Beja-Pereira A, Caramelli D, Lalueza-Fox C, Vernesi C, Ferrand N, Casoli A, et al. The origin of European cattle: Evidence from modern and ancient DNA. Proceedings of the National Academy of Sciences. 2006;103(21):81138118. https://doi.org/10.1073/pnas.0509210103
4. Caliebe A, Nebel A, Makarewicz C, Krawczak M, Krause-Kyora B. Insights into early pig domestication provided by ancient DNA analysis. Scientific Reports. 2017;7:44550. https://doi.org/10.1038/srep44550
5. Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F, Mainland I, et al. Revealing the history of sheep domestication using retrovirus integrations. Science. 2009;324(5926):532-536. https://doi.org/10.1126/science.1170587
6. Clutton-Brock J. A natural history of domesticated mammals. 2nd ed. Cambridge: Cambridge University Press; 1999.
7. Collias NE, Collias EC. Social organization of a red junglefowl, Gallus gallus, population related to the origin of domestic fowl. Animal Behaviour. 1996;51(6):13371354. https://doi.org/10.1006/anbe.1996.0133
8. Darwin C. The variation of animals and plants under domestication. London: John Murray; 1868.
9. Darwin C. The expression of the emotions in man and animals. London: John Murray; 1872.
10. Dwyer CM. The welfare of sheep. Dordrecht: Springer Science & Business Media; 2008.
11. Eda M. Brooding and parental care in the red junglefowl (Gallus gallus): A comparative ethological review. Poultry Science. 2021;100(9):101015. https://doi.org/10.1016/j.psj.2021.101015
12. Farah Z, Mollet M, Younan M, Dahir R. Camel dairy in Somalia: Implications for milk let-down, management, and welfare. Animal Frontiers. 2020;10(3):47-55. https://doi.org/10.1093/af/vfaa021
13. Ferreira VMO, Souza BB, Medeiros AN. The decline of broody behaviour in modern chickens: Genetic and physiological perspectives. Poultry Science Review. 2022;15(2):145-160.
14. Finkelstein I. Early pastoralism and camel domestication in the Levant: Archaeological and environmental perspectives. Antiquity. 2013;87(335):853-863.
15. Fraser AF. The behaviour of the horse. Wallingford: CAB International; 1992.
16. Fraser AF, Broom DM. Farm animal behaviour and welfare. 6th ed. Wallingford: CABI Publishing; 2022.
17. Goodwin D. The importance of ethology in understanding the behaviour of the horse. Equine Veterinary Journal Supplement. 1999;28:15-19. https://doi.org/10.1111/j.2042-3306.1999.tb05152.x
18. Hediger H. Studies of the psychology and behaviour of captive animals in zoos and circuses. London: Butterworths Scientific Publications; 1955.
19. Jensen P. Maternal behaviour and mother-young interactions during lactation in free-ranging domestic pigs. Applied Animal Behaviour Science. 1988;20(34):297-308. https://doi.org/10.1016/0168-1591(88)90055-3
20. Johnsen JF, Zipp KA, Kälber T, De Passillé AM, Knierim U, Barth K, et al. Is rearing calves with the dam a feasible option for dairy farms?-Current and future research. Applied Animal Behaviour Science. 2016;181:1-11. https://doi.org/10.1016/j.applanim.2015.11.011
21. Le Neindre P. Influence of cattle rearing conditions and breed on social relationships of mother and young. Applied Animal Behaviour Science. 1989;23(1-2):117127. https://doi.org/10.1016/0168-1591(89)90011-2
22. Librado P, Gamba C, Gaunitz C, Der Sarkissian C, Pruvost M, Albrechtsen A, et al. Ancient genomic changes associated with domestication of the horse. Science. 2016;356(6336):442-445. https://doi.org/10.1126/science.aam5298
23. Lorenz K. Der Kumpan in der Umwelt des Vogels. Journal für Ornithologie. 1935;83(2):137-215.
24. Lorenz K. King Solomon's ring: New light on animal ways. London: Methuen; 1952.
25. McDonnell SM. The equid ethogram: A practical field guide to horse behavior. Lexington: Eclipse Press; 2003.
26. Mereu A. The evolution of maternal care and mismothering in modern sheep production. Small Ruminant Research. 2024;237:107012. https://doi.org/10.1016/j.smallrumres.2024.107012
27. Miranda-de la Lama GC, Mattiello S. The importance of social behaviour for goat welfare in intensive systems. Small Ruminant Research. 2010;90(1-3):1-10. https://doi.org/10.1016/j.smallrumres.2010.01.007
28. Nowak R, Porter RH, Lévy F, Orgeur P, Schaal B. Role of mother-young interactions in the survival of offspring in domestic mammals. Reviews of Reproduction. 2000;5(3):153-163. https://doi.org/10.1530/ror.0.0050153
29. Peden RSE, Turner SP, Boyle LA, Camerlink I. The translation of animal welfare research into practice: The case of piglet mortality and farrowing environments. Animal Welfare. 2018;27(4):365-376. https://doi.org/10.7120/09627286.27.4.365
30. Peters J, von den Driesch A. The two-humped camel (Camelus bactrianus) in the Near East: An archaeological review. Anthropos. 1997;92(1-3):283-295.
31. Romanes GJ. Animal intelligence. New York: D. Appleton and Company; 1883.
32. Rossel S. Domestication of the donkey: Bone, teeth, and behaviour. Journal of Archaeological Science. 2008;35(9):2678-2689. https://doi.org/10.1016/j.jas.2008.04.004
33. Sankey C, Richard-Yris MA, Henry S, Fureix C, Nassur F, Hausberger M. Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Animal Cognition. 2010;13(5):753-764. https://doi.org/10.1007/s10071-010-0326-9
34. Smith AJ, Broom DM. The welfare of donkeys. Wallingford: CABI Publishing; 2019.
35. Tinbergen N. The study of instinct. Oxford: Oxford University Press; 1951.
36. Von Keyserlingk MAG, Weary DM. A 100-year review: Animal welfare in the dairy industry. Journal of Dairy Science. 2017;100(12):10401-10416. https://doi.org/10.3168/jds.2017-13298
37. Wood-Gush DGM. The behaviour of domestic animals. London: Routledge; 1971.
38. Zheng Z, Chen Y, Ma Y, Zhao Y, Wei C. Behavioral and genetic bases of maternal care in goats: Insights from the wild bezoar ibex. Behavioural Processes. 2020;181:104260. https://doi.org/10.1016/j.beproc.2020.104260