Abstract
In the rapidly expanding field of comparative thanatology, reports from a wide range of taxa suggest that some aspects of a concept of death may be shared by many non-human species. In horses, there are only a few anecdotal reports on behaviors toward dead conspecifics, mostly concerning domestic individuals. Here, we describe the case of a 2-month-old, free-ranging male foal that died around 12 h after being found severely injured due to a presumed wolf attack, focusing on other individuals’ reactions to the dying foal. We also placed camera traps near horse carcasses to investigate reactions by other horses. Kin and non-kin of both sexes showed unusual interest in the dying foal. However, horses appeared to avoid dead conspecifics. Recording individual reactions to dead and dying conspecifics in naturalistic settings will enhance our knowledge about death-related behaviors in horses, allowing comparisons with other species that have been more thoroughly studied, to understand the evolutionary basis of these behaviors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Álvares F (2011) Wolf ecology and conservation in northwest Portugal. PhD thesis in biology (conservation biology), University of Lisbon (in Portuguese)
Anderson JR (2011) A primatological perspective on death. Am J Primatol 73:410–414
Anderson JR (2016) Comparative thanatology. Curr Biol 26:R553–R556
Appleby R, Smith B, Jones D (2013) Observations of a free-ranging adult female dingo (Canis dingo) and littermates’ responses to the death of a pup. Behav Proc 96:42–46. https://doi.org/10.1016/j.beproc.2013.02.016
Austin KS, Bohorquez A, Grigg E, Green D, Allen S, Markowitz H (2001) Observations of epimeletic behavior in northern Pacific harbor seal mothers toward their dead pups at Castro Rocks, San Francisco Bay, California. In: Abstracts in the 14th biennial conference on the biology of marine mammals, Vancouver, p 12
Bearzi G, Eddy L, Piwetz S, Reggente MAL, Cozzi B (2017) Cetacean behavior toward the dead and dying. In: Vonk J, Shackelford TK (eds) Encyclopedia of animal cognition and behaviour. Springer International Publishing, Berlin, pp 1–30. https://doi.org/10.1007/978-3-319-47829-6
Bercovitch FB (2012) Giraffe cow reaction to the death of her newborn calf. Afr J Ecol 51:376–379. https://doi.org/10.1111/aje.12016
Bere R (1966) The African elephant. Golden Press, New York
Berger J (1986) Wild horses of the great basin. University of Chicago Press, Chicago
Biro D, Humle T, Koops K, Sousa C, Hayashi M, Matsuzawa T (2010) Chimpanzee mothers at Bossou Guinea carry the mummified remains of their dead infants. Curr Biol 20:351–352. https://doi.org/10.1016/j.cub.2010.02.031
Byers JA (1984) Play in ungulates. In: Smith PK (ed) Play in animals and humans. Blackwell Scientific, Oxford, pp 43–65
Byers JA, Walker C (1995) Refining the motor training hypothesis for the evolution of play. Am Nat 146(1):25–40
Byrne RW, Bates LA (2007) Sociality, evolution and cognition. Curr Biol 17(16):R714–R723
Carter K (2011) Interesting giraffe behavior in Etosha National Park. Giraffa Newsl 5:14–15
Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. PNAS 106(33):13850–13853
Cronin KA, van Leeuwen EJC, Mulenga IC, Bodamer MD (2011) Behavioral response of a chimpanzee mother toward her dead infant. Am J Primatol 73:415–421. https://doi.org/10.1002/ajp.20927
de Kort D, Altrichter M, Cortez S, Camino M (2018) Collared peccary (Pecari tajacu) behavioral reactions toward a dead member of the herd. Ethology 124:131–134. https://doi.org/10.1111/eth.12709
Dickinson GE, Hoffmann HC (2016) The difference between dead and away: an exploratory study of behavior change during companion animal euthanasia. J Vet Behav Clin Appl Res 15:61–65
Douglas-Hamilton I, Bhalla S, Wittemyer G, Vollrath F (2006) Behavioural reactions of elephants towards a dying and deceased matriarch. Appl Anim Behav Sci 100:87–102. https://doi.org/10.1016/j.applanim.2006.04.014
Feh C (2005) Relationships and communication in socially natural horse herds. In: Mills D, McDonnell S (eds) The domestic horse. Cambridge University Press, New York, pp 83–93
Forss SI, Koski SE, van Schaik CP (2017) Explaining the paradox of neophobic explorers: the social information hypothesis. Int J Primatol 38(5):799–822
Gonçalves A, Biro D (2018) Comparative thanatology, an integrative approach: exploring sensory/cognitive aspects of death recognition in vertebrates and invertebrates. Philos Trans R Soc B 373(1754):20170263
Hanggi EB (1999) Categorization learning in horses (Equus caballus). J Comp Psychol 113(3):243–252
Hanggi EB (2003) Discrimination learning based on relative size concepts in horses (Equus caballus). Appl Anim Behav Sci 83:201–213
Hanggi EB, Ingersoll JF (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn 12(3):451–462
Hartman DS (1979) Ecology and behavior of the manatee (Trichechus manatus) in Florida. Spec Pub Am Soc Mammal 5:1–153
Heitor F, Vicente L (2008) Maternal care and foal social relationships in a herd of Sorraia horses: Influence of maternal rank and experience. App Anim Behav Sci 113(1–3):189–205
Kenyon KW (1969) Sea otter in eastern Pacific Ocean. N Am Fauna 68:1–352. https://doi.org/10.3996/nafa.68.0001
King BJ (2013) How animals grieve. The University of Chicago Press, Chicago
Krueger K, Flauger B, Farmer K, Maros K (2010) Horses (Equus caballus) use human local enhancement cues and adjust to human attention. Anim Cogn 14:187–201
Macdonald DW (1991) Running with the fox. Unwin Hyman, London
Marais E (1969) The soul of ape. Atheneum, New York
Marino L, Connor RC, Fordyce RE et al (2007) Cetaceans have complex brains for complex cognition. PLoS Biol 5(5):e139
Matsuzawa T (2017) Horse cognition and behavior from the perspective of primatology. Primates 58:473–477. https://doi.org/10.1007/s10329-017-0632-9
Morais J, Oom MM, Malta-Vacas J, Luís C (2005) Genetic structure of an endangered Portuguese semiferal pony breed, the Garrano. Biochem Genet 43:347–364
Moss C (1988) Elephant memories: thirteen years in the life of an elephant family. William Morrow & Co, New York
Muller Z (2010) The curious incident of the giraffe in the night time. Giraffa Newsl 4:20–23
Murray JH (1871) Travels in Uruguay. Longmans & Co, London
Payne KB (2003) Sources of social complexity in the three elephant species. In: de Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, pp 81–83
Pereira ME (2002) Juvenility in animals. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 17–27
Pierce J (2013) The dying animal. J Bioethical Inq 10(4):469–478
Proops L, McComb K (2012) Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc B Biol Sci 279:3131–3138
Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). PNAS 106(3):947–951
Rasa OAE (1983) A case of invalid care in wild dwarf mongooses. Zeits Tierpsychol 62(3):235–240
Ringhofer M, Yamamoto S (2017) Domestic horses send signals to humans when they are faced with an unsolvable task. Anim Cogn 20:397–405
Ringhofer M, Inoue S, Mendonça RS, Pereira C, Matsuzawa T, Hirata S, Yamamoto S (2017) Comparison of the social systems of primates and feral horses: data from a newly established horse research site on Serra D’Arga, northern Portugal. Primates 58:479–484. https://doi.org/10.1007/s10329-017-0614-y
Rosenfeld M (1983) Two female northwest Atlantic harbor seals (P. vitulina concolor) carry dead pups with them for over two weeks—some unusual behavior in the field and its implication for a further understanding of maternal investment. In: Abstract 5th biennial conf. on biology of marine mammals, Boston, p 87
Schaller GB (1972) The Serengetti lion. University of Chicago Press, Chicago
Siebenaler JB, Caldwell DK (1956) Cooperation among adult dolphins. J Mammal 37(1):126–128
Smith AV, Proops L, Grounds K, Wathan J, McComb K (2016) Functionally relevant responses to human facial expressions of emotion in the domestic horse (Equus caballus). Biol Lett 12:20150907
Sugiyama Y, Kurita H, Matsui T, Kimoto S, Shimomura T (2009) Carrying of dead infants by Japanese macaque (Macaca fuscata) mothers. Anthropol Sci 117(2):11–39
Takimoto A, Hori Y, Fujita K (2016) Horses (Equus caballus) adaptively change the modality of their begging behavior as a function of human attentional states. Psychologia 59:100–111
Waller BM, Whitehouse J, Micheletta J (2016) Macaques can predict social outcomes from facial expressions. Anim Cogn 19:1031–1036
Waring GH (2003) Horse behavior. William Andrew Publishing, Norwich, pp 283–300
Wathan J, Proops L, Grounds K, McComb K (2016) Horses discriminate between facial expressions of conspecifics. Sci Rep 6:38322. https://doi.org/10.1038/srep38322
Watson CFI, Matsuzawa T (2018) Behaviour of nonhuman primate mothers toward their dead infants: uncovering mechanisms. Philos Trans R Soc B 373:20170261. https://doi.org/10.1098/rstb.2017.0261
Acknowledgements
A special thanks to Viana do Castelo city for supporting our project. We also thank Dr. Tetsuro Matsuzawa, Dr. Carlos Pereira, Lourenço Almada, Dr. Ricardo Carvalhido and the villagers in Montaria for their support during our stay. We are very grateful to Dr. James R. Anderson, Dr. Shinya Yamamoto, and anonymous reviewers for their comments on an earlier version of this manuscript. The study was financially supported by JSPS core-to-core CCSN and JSPS-LGP-U04, and MEXT No. 16H06283 to Tetsuro Matsuzawa, KAKENHI Nos. 15H01619, 15H05309, 17H0582, and Kyoto University SPIRITS to Shinya Yamamoto, and KAKENHI No. 18K18342 to Monamie Ringhofer.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10329_2019_728_MOESM2_ESM.png
Supplementary material 2 (PNG 1638 kb) Supplementary Fig. 1 Distances between Nabari, the mother (black) and Tsu, the male (blue) and the injured foal during a 1-h observation in the morning starting at 11.50. The pictures in the plot represent interactions occurring at minutes 2 (Nabari feeding near the foal) and 10 (Tsu sniffing the foal)
10329_2019_728_MOESM3_ESM.png
Supplementary material 3 (PNG 2440 kb) Supplementary Fig. 2 Distances between Nabari, the mother (black) and Usa/Saito, bachelor males (purple) and the injured foal during a 30-min observation period starting at 11.50. The pictures in the plot represent the interactions occurring at the minute 8 (Nabari threatening to kick Usa)
10329_2019_728_MOESM4_ESM.png
Supplementary material 4 (PNG 2759 kb) Supplementary Fig. 3 Three horses from Zama (male) and Kamakura (male) group vigilant toward the carcass (A). Kamakura (male) sniffing the area nearby the carcass (B)
Supplementary material 5 (MP4 270422 kb)
Supplementary material 6 (MP4 248311 kb)
Supplementary material 7 (MP4 329983 kb)
Supplementary material 8 (MP4 329873 kb)
Supplementary material 9 (MP4 246970 kb)
About this article
Cite this article
Mendonça, R.S., Ringhofer, M., Pinto, P. et al. Feral horses’ (Equus ferus caballus) behavior toward dying and dead conspecifics. Primates 61, 49–54 (2020). https://doi.org/10.1007/s10329-019-00728-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-019-00728-x