Effect of social organisation on interspecific differences in overmarking behaviour of foals in African equids

  • Jan PluháčekEmail author
  • Vladimíra Tučková
  • Radka Šárová
  • Sarah R. B. King
Original Paper


Overmarking remains an unstudied topic in juvenile mammals. We have previously documented a very high rate of overmarking by foals in four captive African equid species: mountain zebra (Equus zebra), plains zebra (Equus quagga), Grévy’s zebra (Equus grevyi), and African wild ass (Equus africanus). African equids vary interspecifically in their social organisation. Since differences in social organisation affect many mammalian behaviours, in this study we investigated interspecific differences in overmarking behaviour of foals, analysing only cases where elimination of any other individual was explored by a foal. We hypothesised that the pattern of overmarking by foals should reflect either differences in social organisation of the species or phylogenetic relations among them. We found that in all species very young foals explored mostly maternal eliminations, and this preference declined with increasing age of the foal and reflected the social organisation of the species; the highest overmarking rate was in species with high intragroup aggression (mountain zebra) and lowest in species with low intragroup aggression and which form crèches (African wild ass). Similarly, the rate of overmarking of the mother, as opposed to other herdmates, was associated with social organisation of the respective species. Thus, we found interspecific differences in overmarking by foals, which were associated with variability in social organisation. Since we also revealed differences between African wild ass and zebra behaviour in early stages of ontogeny, we cannot refute the effect of phylogeny on overmarking behaviour. Additionally, our results supported the identity sharing hypothesis as an explanation of overmarking.


Equus Interspecific differences Marking behaviour Olfactory communication Social organisation Zebra African wild ass 



The authors gratefully acknowledge the assistance of the Zoological Garden staff at Dvůr Králové, Brno, Liberec, Ostrava, and Ústí nad Labem, in particular Luděk Čulík, Markéta Čulíková, Aleš Kopecký, Jiří Soumar, Miroslava Kubelková, Miroslava Doležalová, Pavel Moucha, Radek Hlávka, Lubomír Melichar, Jiří Vítek, Petra Padalíková, Pavel Král, Jaroslav Novák, Rostislav Střižík, Eva Zajoncová, and Lenka Málcová. This work was supported by the Ministry of Agriculture of the Czech Republic (MZE-RO0719) and by Grant no. 2011/008 of the Student Grant Agency of the University of South Bohemia.

Compliance for ethical standard

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The study was designed according to laws of the European Union and Czech Republic.


  1. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267PubMedPubMedCentralGoogle Scholar
  2. Bekoff M, Wells MC (1981) Behavioral budgeting by wild coyotes—the influence of food resources and social organisation. Anim Behav 29:794–801CrossRefGoogle Scholar
  3. Berger J (1988) Social systems, resources and phylogenetic inertia: an experimental test and its limitations. In: Slobodchikoff CN (ed) The ecology of social behaviour. Academic Press, London, pp 157–186CrossRefGoogle Scholar
  4. Blank D, Ruckstuhl K, Yang WK (2015) The economics of scent marking with urine and feces in goitered gazelle (Gazella subgutturosa). Mammal Res 60:51–60CrossRefGoogle Scholar
  5. Brinck C, Erlinge S, Sandell M (1983) Anal sac secretion in mustelids—a comparison. J Chem Ecol 9:727–745PubMedCrossRefGoogle Scholar
  6. Brown RE, Macdonald DW (1985) Social odours in mammals, vol 2. Clarendon Press, OxfordGoogle Scholar
  7. Caine NG, Marra SL (1988) Vigilance and social organisation in two species of primates. Anim Behav 36:897–904CrossRefGoogle Scholar
  8. Crowell-Davis SL, Houpt KA (1985) The ontogeny of flehmen in horses. Anim Behav 33:739–745CrossRefGoogle Scholar
  9. Ferkin MH (1999) Meadow voles (Microtus pennsylvanicus, Arvicolidae) over-mark and adjacent-mark the scent marks of same-sex conspecifics. Ethology 105:825–837CrossRefGoogle Scholar
  10. Ferkin MH, Pierce AA (2007) Perspectives on over-marking: is it good to be on top? J Ethol 25:107–116CrossRefGoogle Scholar
  11. Ferkin MH, Leonard ST, Bartos K, Schmick MK (2001) Meadow voles and prairie voles differ in the length of time they prefer the top-scent donor of an over-mark. Ethology 107:1099–1114CrossRefGoogle Scholar
  12. Ferkin MH, Lee DN, Leonard ST (2004) The reproductive state of female voles affects their scent marking behavior and the responses of male conspecifics to such marks. Ethology 110:257–272CrossRefGoogle Scholar
  13. Ganslosser A, Dellert B (1997) Experimental alternations of food distribution in two species of captive equids (Equus burchelli and Equus hemionus). Ethol Ecol Evol 9:1–17CrossRefGoogle Scholar
  14. Ginsberg JR (1989) The ecology of female behaviour and male reproductive success in the Grevy’s zebra, Equus grevyi. In: Maloiy GMO (ed) Jewell PA. Symp Zool Soc Lond Clarendon Press, Oxford, pp 89–110Google Scholar
  15. Isbell LA, Young TP (1993) Social and ecological influences on activity budgets of vervet monkeys, and their implications for group living. Behavl Ecol Sociobiol 32:377–385CrossRefGoogle Scholar
  16. Johnson RP (1973) Scent marking in mammals. Anim Behav 21:521–535CrossRefGoogle Scholar
  17. Johnston RE (2008) Individual odors and social communication: individual recognition, kin recognition, and scent over-marking. In: Brockmann HJ, Roper TJ, Naguib M, Wynne-Edwards KE, Barnard C, Mitani JC (eds) Advances in the Study of Behavior, vol 38. Academic Press, New York, pp 439–505Google Scholar
  18. Jordan NR, Manser MB, Mwanguhya F, Kyabulima S, Ruedi P, Cant MA (2011a) Scent marking in wild banded mongooses: 1. Sex-specific scents and overmarking. Anim Behav 81:31–42CrossRefGoogle Scholar
  19. Jordan NR, Mwanguhya F, Furrer RD, Kyabulima S, Ruedi P, Cant MA (2011b) Scent marking in wild banded mongooses: 2. Intrasexual overmarking and competition between males. Anim Behav 81:43–50CrossRefGoogle Scholar
  20. Jordan NR, Mwanguhya F, Kyabulima S, Ruedi P, Hodge SJ, Cant MA (2011c) Scent marking in wild banded mongooses: 3. Intrasexual overmarking in females. Anim Behav 81:51–60CrossRefGoogle Scholar
  21. Joubert E (1972) The social organisation and associated behaviour in the Hartmann zebra Equus zebra hartmannae. Madoqua SerI 6:17–56Google Scholar
  22. Kimura R (2000) Relationship of the type of social organization to scent-marking and mutual-grooming behaviour in Grevy’s (Equus grevyi) and Grant’s zebra (Equus burchelli bohmi). J Equin Sci 11:91–98CrossRefGoogle Scholar
  23. Kimura R (2001) Volatile substances in feces, urine and urine/marked feces of feral horses. Can J Anim Sci 81:411–420CrossRefGoogle Scholar
  24. Klingel H (1972) Social behaviour of African Equidae. Zool Afr 7:175–185CrossRefGoogle Scholar
  25. Klingel H (1974) Soziale Organisation und Verhalten des Grevy-Zebras (Equus grevyi). Z Tierpsychol 36:36–70Google Scholar
  26. Klingel H (1975) A comparison of the social behaviour of the Equidae. In: Geist V, Walther F (eds) The papers of an international symposium on the behaviour of ungulates and its relation to management. IUCN, pp 124–132Google Scholar
  27. Klingel H (1977) Observations on social organization and behaviour of African and Asiatic wild assess (Equus africanus and E. hemionus). Z Tierpsychol 44:323–331PubMedCrossRefPubMedCentralGoogle Scholar
  28. Koomen R, Herrmann E (2018) The effects of social context and food abundance on chimpanzee feeding competition. Am J Primatol 80:e22734CrossRefGoogle Scholar
  29. Krueger K, Flauger B (2011) Olfactory recognition of individual competitors by means of faeces in horse (Equus caballus). Anim Cogn 14:245–257PubMedCrossRefGoogle Scholar
  30. Krüger K, Gaillard C, Stranzinger G, Rieder S (2005) Phylogenetic analysis and species allocation of individual equids using microsatellite data. J Anim Breed Gen 122:78–86CrossRefGoogle Scholar
  31. Liang KY, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13–22CrossRefGoogle Scholar
  32. Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, CambridgeGoogle Scholar
  33. Macdonald DW (1980) Patterns of scent marking with urine and faeces amongst carnivore communities. Symp Zool Soc Lond 45:107–139Google Scholar
  34. Macdonald DW (1985) The carnivores: order Carnivora. In: Brown RE, Macdonald DW (eds) Social odours in mammals, vol 2. Clarendon Press, Oxford, pp 619–722Google Scholar
  35. Maestripieri D (1994) Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides) II. The social environment. Behaviour 131:97–113CrossRefGoogle Scholar
  36. McGuire B, Novak M (1984) A comparison of maternal behavior in the meadow vole (Microtus pennsylvanicus), prairie vole (Microtus ochrogaster) and pine vole (Microtus pinetorum). Anim Behav 32:1132–1141CrossRefGoogle Scholar
  37. McGuire B, Vermeylen F, Bemis WE (2011) Suckling behaviour in three species of voles. Behaviour 148:551–573CrossRefGoogle Scholar
  38. Moehlman PD (1985) The odd-toed ungulates: order Perrisodactyla. In: Brown RE, Macdonald DW (eds) Social odours in mammals, vol 2. Clarendon Press, Oxford, pp 531–549Google Scholar
  39. Moehlman PD (1998) Behavioral patterns and communication in feral asses (Equus africanus). Appl Anim Behav Sci 60:125–169CrossRefGoogle Scholar
  40. Moehlman PD, Kebede F, Yohannes H (2013) Equus africanus African wild ass. In: Kingdon J, Hoffmann M (eds) Mammals of Africa, vol V. carnivores, pangolines, equids and rhinoceros. Bloomsbury, London, pp 422–428Google Scholar
  41. Müller-Schwarze D (2006) The chemical ecology of vertebrates. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  42. Oakenfull EA, Lim HN, Ryder OA (2000) A survey of equid mitochondrial DNA: implications for the evolution, genetic diversity and conservation of Equus. Conserv Gen 1:341–355CrossRefGoogle Scholar
  43. Olléová M, Pluháček J, King SRB (2012) Effect of social system on allosuckling and adoption in zebras. J Zool 288:127–134CrossRefGoogle Scholar
  44. Palombit RA (2015) Infanticide as sexual conflict: coevolution of male strategies and female counterstrategies. Cold Spring Harbor Perspect Biol 7:a017640CrossRefGoogle Scholar
  45. Penzhorn BL (1984) A long-term study of social organization and behaviour of Cape mountain zebra (Equus zebra zebra). Z Tierpsychol 64:97–146CrossRefGoogle Scholar
  46. Pluháček J, Bartoš L, Víchová J (2006) Variation in incidence of male infanticide within subspecies of plains zebra (Equus burchelli). J Mammal 87:35–40CrossRefGoogle Scholar
  47. Pluháček J, Bartoš L, Doležalová M, Bartošová-Víchová J (2007) Sex of the foetus determines the time of weaning of the previous offspring of captive plains zebra (Equus burchelli). Appl Anim Behav Sci 105:192–204CrossRefGoogle Scholar
  48. Pluháček J, Olléová M, Bartošová J, Bartoš L (2012) Effect of ecological adaptation on suckling behaviour in three zebra species. Behaviour 149:1395–1411CrossRefGoogle Scholar
  49. Pluháček J, Olléová M, Bartoš L, Bartošová J (2014) Time spent suckling is affected by different social organization in three zebra species. J Zool 292:10–17CrossRefGoogle Scholar
  50. Pluháček J, Tučková V, King SRB, Šárová R (2019a) Test of four hypotheses to explain the function of overmarking in foals of four equid species. Anim Cogn 22:231–241PubMedCrossRefGoogle Scholar
  51. Pluháček J, Tučková V, King SRB (2019b) Overmarking behaviour of zebra males: no scent masking, but a group cohesion function across three species. Behav Ecol Sociobiol 73:137CrossRefGoogle Scholar
  52. Policht R, Karadžos A, Frynta D (2011) Comparative analysis of long-range calls in equid stallions (Equidae): are acoustic parameters related to social organization? Afr Zool 46:18–26CrossRefGoogle Scholar
  53. Ralls K (1971) Mammalian scent marking. Science 171:443–449PubMedCrossRefPubMedCentralGoogle Scholar
  54. Roberts SC (2007) Scent marking. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 255–266Google Scholar
  55. Rubenstein DI (1989) The life history and social organization in arid adapted ungulates. J Arid Environ 17:145–156CrossRefGoogle Scholar
  56. Steiner CC, Ryder OA (2011) Molecular phylogeny and evolution of the Perissodactyla. Zool J Lin Soc 163:1289–1303CrossRefGoogle Scholar
  57. Steiner CC, Mitelberg A, Tursi R, Ryder OA (2012) Molecular phylogeny of extant equids and effects of ancestral polymorphism in resolving species-level phylogenies. Mol Phyl Evol 65:573–581CrossRefGoogle Scholar
  58. Sundaresan SR, Fischhoff IR, Dushoff J, Rubenstein DI (2007) Network metrics reveal differences in social organization between two fission-fusion species, Grevy’s zebra and onager. Oecologia 151:140–149PubMedCrossRefPubMedCentralGoogle Scholar
  59. Thierry B (1985) Social development in three species of macaques (Macaca mulatta, M. fascicularis, M. tonkeana): a preliminary report on the first ten weeks of life. Behav Proc 11:89–95CrossRefGoogle Scholar
  60. Tučková V, Šárová R, Bartošová J, King SRB, Pluháček J (2018) Overmarking by adult females in four equid species: social bonds and group cohesion. J Zool 306:180–188CrossRefGoogle Scholar
  61. Turner JW, Perkins A, Kirkpatrick JF (1981) Elimination marking behavior in feral horses. Can J Zool 59:1561–1566CrossRefGoogle Scholar
  62. Tyler SJ (1972) The behaviour and social organisation of the New Forest ponies. Anim Behav Monogr 5:85–196CrossRefGoogle Scholar
  63. Vilstrup JT, Seguin-Orlando A, Stiller M, Ginolhac A, Raghavan M, Nielsen SCA, Weinstock J, Froese D, Vasiliev SK, Ovodov ND, Clary J, Helgen KM, Fleischer RC, Cooper A, Shapiro B, Orlando L (2013) Mitochondrial phylogenomics of modern and ancient equids. Plos One 8:e55950PubMedPubMedCentralCrossRefGoogle Scholar
  64. Williams SD (2013) Equus grevyi Grévy’s zebra. In: Kingdon J, Hoffmann M (eds) Mammals of Africa, vol V. Carnivores, pangolines, equids and rhinoceros. Bloomsbury, London, pp 422–428Google Scholar
  65. Woodward JRL, Schmick MK, Ferkin MH (1999) Response of prairie voles, Microtus ochrogaster (Rodentia, Arvicolidae) to scent over-marks of two same-sex conspecifics: a test of the scent masking hypothesis. Ethology 105:1009–1017CrossRefGoogle Scholar
  66. Woodward JRL, Bartos K, Ferkin MH (2000) Meadow voles (Microtus pennsylvanicus) and prairie voles (Microtus ochrogaster) differ in their responses to over-marks from opposite- and same-sex conspecifics. Ethology 106:979–992CrossRefGoogle Scholar
  67. Wright S (1922) Coefficients of inbreeding and relationship. Am Nat 56:330–338CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of EthologyInstitute of Animal SciencePraha-UhříněvesCzech Republic
  2. 2.Ostrava ZooOstravaCzech Republic
  3. 3.Department of Biology and Ecology, Faculty of ScienceUniversity of OstravaOstravaCzech Republic
  4. 4.Department of Zoology, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  5. 5.Natural Resource Ecology Laboratory, Warner College of Natural ResourcesColorado State UniversityFort CollinsUSA

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