This paper addresses the biosemiotic dimensions of human relationship with captive animals and aims to uncover how these factors influence handling practices and human-animal interactions within zoological gardens. Zoological gardens are quintessential hybrid environments, and as such, they are places of interspecies interactions and mutual influences. These interactions are profoundly shaped by human attitudes towards animals. The roots of these attitudes can be found at the cultural and institutional levels (how particular animal species are culturally perceived and managed in zoos) as well as at the biosemiotic level (similarities between Umwelten). Previous studies have suggested that keepers’ attitudes towards animals have direct influences on their handling style and, consequently, have an impact on animals’ perception of keepers and other humans. This suggests that the type of relationship between keepers and animals can translate into handling styles that may affect animals’ perceptions of humans and worsen or improve their welfare. In this paper, we present a case study involving chimpanzees’ keepers at the Tallinn Zoological Gardens (Estonia). A series of interviews were conducted, which aimed to uncover the way keepers understand their relationships with captive animals and how this influences handling. This work offers a comparative approach by bringing forward the experiences of keepers who work with various animal species belonging to different taxa (Cebuella pygmae, Pan troglodytes) and class (Mammalia and Reptilia, i.e. Crocodylus porosus). Such an approach aims to highlight the biosemiotic factors behind the emergence of different types of keeper-animal relationships. We expect to uncover whether extremely different Umwelten may shape human-animal bonds. By highlighting the agency of animals in daily activities and work routine, we also aim to initiate a discussion on the way animals influence handling practices within zoological gardens. Our objective is to understand how individual animals influence handling practices within zoological gardens.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
The zoo was founded on the 25th August 1939 and was officially recognised as a member of the World Association of Zoos and Aquariums (WAZA) in 1989, earlier than any other zoo in the Soviet Union.
Old man, in Estonian. The name was given to the crocodile when he was still a hatchling. Keepers are not sure where he got his name, however K1 deemed it “offensive”.
The expression translates into English as “zero degree” and could mean the “rock bottom” or the “starting point” of a hybrid community. [From the translator’s note (Lestel 2014: 72)]
This idea is best summarised by referring to K3’s own words: “[…] marmosets live in a group; they think as a troop”.
Pino was ill for some time and needed medical attention, which meant that keepers had to administer eye drops multiple times per day. This was easily achieved because he did not offer resistance but collaborated with keepers.
K1 and K3 both confused pygmy marmosets with tamarins when talking about their work routine. It is unclear whether they perceive the two species as having little intraspecific differences. Estonian and Russian have separate words for both species.
Verbatim transcription of K3’s words. The keeper explained that they liken “sudden bursts of anger” that characterise chimpanzees’ behaviour to unpredictable people. Rather than dehumanising people with disabilities, K3 intended to humanise chimpanzees.
These features must not be understood as exclusive factors influencing human interest, as the picture presented here is rather a simplified one. Cultural variations also have a strong influence on biologically dictated preferences, as acknowledged in our introduction.
Marmosets can hear frequencies extending to 30 kHz, which goes beyond the average human hearing range (20 Hz–20 kHz).
Batt, S. (2009). Human attitudes towards animals in relation to species similarity to humans: A multivariate approach. Bioscience Horizons, 2(2), 180–190.
Beatson, R. M., & Halloran, M. J. (2007). Humans rule! The effects of creatureliness reminders, mortality salience and self-esteem on attitudes towards animals. British Journal of Social Psychology, 46(3), 619–632. https://doi.org/10.1348/014466606X147753.
Brien, M. L., Webb, G. J., Christian, K. A., Lang, J. W., & McGuinness, K. A. (2013). Born to be bad: Agonistic behaviour in hatchling saltwater crocodiles (Crocodylus porosus). Behaviour, 150(7), 737–762. https://doi.org/10.1163/1568539X-00003078.
Burghardt, G. M. (2013). Environmental enrichment and cognitive complexity in reptiles and amphibians: Concepts, review, and implications for captive populations. Applied Animal Behaviour Science, 147(3–4), 286–298. https://doi.org/10.1016/j.applanim.2013.04.013.
Carder, G., & Semple, S. (2008). Visitor effects on anxiety in two captive groups of western lowland gorillas. Applied Animal Behaviour Science, 115(3–4), 211–220. https://doi.org/10.1016/j.applanim.2008.06.001.
Carrasco, L., Colell, M., Calvo, M., Abeló, M. T., Velasco, M., & Posada, S. (2009). Benefits of training/playing therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla). Animal Welfare, 18(1), 9–19.
Cerrone, M. (2018). Umwelt and ape language experiments: On the role of iconicity in the human-ape pidgin language. Biosemiotics, 11(1), 41–63. https://doi.org/10.1007/s12304-018-9312-4.
Cerrone, M. (forthcoming). Keepers as social companions: tactile communication and social enrichment for captive apes. Sign Systems Studies, 47, 2.
Chamove, A. S., Hosey, G. R., & Schaetzel, P. (1988). Visitors excite primates in zoos. Zoo Biology, 7(4), 359–369. https://doi.org/10.1002/zoo.1430070407.
Claxton, A. M. (2011). The potential of the human-animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Applied Animal Behaviour Science, 133(1–2), 1–10. https://doi.org/10.1016/j.applanim.2011.03.002.
Czech, B., Krausman, P. R., & Borkhataria, R. (1998). Social construction, political power, and the allocation of benefits to endangered species. Conservation Biology, 12(5), 1103–1112. https://doi.org/10.1046/j.1523-1739.1998.97253.x.
Davey, G. (2007). Visitors’ effects on the welfare of animals in the zoo: A review. Journal of Applied Animal Welfare Science, 10(2), 169–183. https://doi.org/10.1080/10888700701313595.
De La Torre, S., & Snowdon, C. T. (2002). Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea. Animal Behaviour, 63(5), 847–856. https://doi.org/10.1006/anbe.2001.1978.
Dobson, S. D. (2009). Socioecological correlates of facial mobility in nonhuman anthropoids. American Journal of Physical Anthropology, 139(3), 413–420. https://doi.org/10.1002/ajpa.21007.
Drummond, H. (2006). Dominance in vertebrate broods and litters. The Quarterly Review of Biology, 81(1), 3–32. https://doi.org/10.1086/503922.
Dydynski, J., & Mäekivi, N. (2018). Multisensory perception of cuteness in mascots and zoo animals. International Journal of Marketing Semiotics, 6(1), 2–25 https://ijms.files.wordpress.com/2018/09/ijms-vol-vi-2018_dydynski.pdf.
Elowson, A. M., & Snowdon, C. T. (1994). Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Animal Behaviour, 47(6), 1267–1277. https://doi.org/10.1006/anbe.1994.1175.
European Association of Zoos and Aquaria. (2014). EAZA standards for the accommodation and care of animals in zoos and aquaria. Retrieved from http://www.eaza.net/assets/Uploads/Standards-and-policies/Standards-for-the-Accommodation-and-Care-of-Animals-2014.pdf
Fernandez, E. J., Tamborski, M. A., Pickens, S. R., & Timberlake, W. (2009). Animal-visitor interactions in the modern zoo: Conflicts and interventions. Applied Animal Behaviour Science, 120(1–2), 1–8. https://doi.org/10.1016/j.applanim.2009.06.002.
Ferreira, M. I. A., & Caldas, M. G. (2013). The concept of Umwelt overlap and its application to cooperative action in multi-agent systems. Biosemiotics, 6(3), 497–514. https://doi.org/10.1007/s12304-013-9185-5.
Hampson, J., & Steven, H. (2019). Electrical trade principles (5th ed.). South Melbourne: Cengage Learning Australia Pty Limited.
Hediger, H. (1968). The psychology and behaviour of animals in zoos and circuses. New York: Dover Publications.
Heymann, E. W., & Soini, P. (1999). Offspring number in pygmy marmosets, Cebuella pygmaea, in relation to group size and the number of adult males. Behavioral Ecology and Sociobiology, 46(6), 400–404. https://doi.org/10.1007/s002650050635.
Hosey, G. R. (2000). Zoo animals and their human audiences: What is the visitor effect? Animal Welfare, 9(4), 343–357.
Hosey, G. R. (2008). A preliminary model of human-animal relationships in the zoo. Applied Animal Behaviour Science, 109(2–4), 105–127. https://doi.org/10.1016/j.applanim.2007.04.013.
Hosey, G. R., & Melfi, V. (2012). Human-animal bonds between zoo professionals and the animals in their care. Zoo Biology, 31(1), 13–26. https://doi.org/10.1002/zoo.20359.
Hosey, G. R., & Melfi, V. (2015). Are we ignoring neutral and negative human-animal relationships in zoos? Zoo Biology, 34(1), 1–8. https://doi.org/10.1002/zoo.21182.
Kellert, S. R. (1993). Values and perceptions of invertebrates. Conservation Biology, 7(4), 845–855. https://doi.org/10.1046/j.1523-1739.1993.740845.x.
Kissui, B. M. (2008). Livestock predation by lions, leopards, spotted hyenas, and their vulnerability to retaliatory killing in the Maasai steppe, Tanzania. Animal Conservation, 11(5), 422–432. https://doi.org/10.1111/j.1469-1795.2008.00199.x.
Knight, A. J. (2008). “Bats, snakes and spiders, oh my!” how aesthetic and negativistic attitudes, and other concepts predict support for species protection. Journal of Environmental Psychology, 28(1), 94–103. https://doi.org/10.1016/j.jenvp.2007.10.001.
Kuppert, S. (2013). Providing enrichment in captive amphibians and reptiles: Is it important to know their communication? Smithsonian Herpetological Information Service, 142, 1–42.
Lang, J. (1987). Crocodilian behavior: Implications for management. In G. J. W. Webb, C. S. Manolis, & P. J. Whitehead (Eds.), Wildlife management: Crocodile and alligators (pp. 273–294). Sydney: Surrey Beatty.
Lestel, D. (2004). L’animal singulier. Paris: Seuil.
Lestel, D. (2014). Hybrid communities. Angelaki – Journal of the Theoretical Humanities, 19(3), 61–73. https://doi.org/10.1080/0969725X.2014.976049.
Lestel, D., Bussolini, J., & Chrulew, M. (2014). The phenomenology of animal life. Environmental Humanities, 5(1), 125–148. https://doi.org/10.1215/22011919-3615442.
Mäekivi, N. (2016). Modelling ex situ animal behaviour and communication. Biosemiotics, 9(2), 207–226. https://doi.org/10.1007/s12304-016-9264-5.
Mäekivi, N. (2018). The zoological garden as a hybrid environment — A (zoo)semiotic analysis (PhD dissertation). Tartu: University of Tartu Press.
Mäekivi, N., & Maran, T. (2016). Semiotic dimensions of human attitudes towards other animals: A case of zoological gardens. Sign Systems Studies, 44(1–2), 209–230. https://doi.org/10.12697/SSS.2016.44.1-2.12.
Marchesini, R. (2017). Over the human: Post-humanism and the concept of animal epiphany (Vol. 4). Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-62581-2.
Margulis, S. W., Hoyos, C., & Anderson, M. (2003). Effect of felid activity on zoo visitor interest. Zoo Biology, 22(6), 587–599. https://doi.org/10.1002/zoo.10115.
Martin, R. A., & Melfi, V. (2016). A comparison of zoo animal behavior in the presence of familiar and unfamiliar people. Journal of Applied Animal Welfare Science, 19(3), 234–244. https://doi.org/10.1080/10888705.2015.1129907.
Mellen, J. D. (1991). Factors influencing reproductive success in small captive exotic felids (Felis spp.): A multiple regression analysis. Zoo Biology, 10(2), 95–110. https://doi.org/10.1002/zoo.1430100202.
Montanha, J. C., Silva, S. L., & Boere, V. (2009). Comparison of salivary cortisol concentrations in jaguars kept in captivity with differences in exposure to the public. Ciência Rural, 39(6), 1745–1751. https://doi.org/10.1590/s0103-84782009005000089.
Oli, M. K. (1994). Snow leopards and blue sheep in Nepal: Densities and predator: Prey ratio. Journal of Mammalogy, 75(4), 998–1004. https://doi.org/10.2307/1382482.
Quadros, S., Goulart, V. D. L., Passos, L., Vecci, M. A. M., & Young, R. J. (2014). Zoo visitor effect on mammal behaviour: Does noise matter? Applied Animal Behaviour Science, 156, 78–84. https://doi.org/10.1016/j.applanim.2014.04.002.
Rajagopal, T., Archunan, G., & Sekar, M. (2011). Impact of zoo visitors on the fecal cortisol levels and behavior of an endangered species: Indian blackbuck (Antelope Cervicapra L.). Journal of Applied Animal Welfare Science, 14(1), 18–32. https://doi.org/10.1080/10888705.2011.527598.
Santana, S. E., Alfaro, J. L., & Alfaro, M. E. (2012). Adaptive evolution of facial colour patterns in Neotropical primates. Proceedings of the Royal Society B: Biological Sciences, 279(1736), 2204–2211. https://doi.org/10.1098/rspb.2011.2326.
Sellinger, R. L., & Ha, J. C. (2005). The effects of visitor density and intensity on the behavior of two captive jaguars (Panthera onca). Journal of Applied Animal Welfare Science, 8(4), 233–244. https://doi.org/10.1207/s15327604jaws0804_1.
Semeniuk, V., Manolis, C., Webb, G. J. W., & Mawson, P. R. (2011). The saltwater crocodile, Crocodylus porosus Schneider, 1801, in the Kimberley coastal region. Journal of the Royal Society of Western Australia, 94(2), 407–416.
Snowdon, C. T., & Cleveland, J. (1984). “Conversations” among pygmy marmosets. American Journal of Primatology, 7(1), 15–20. https://doi.org/10.1002/ajp.1350070104.
Snowdon, C. T., & Elowson, A. M. (1999). Pygmy marmosets modify call structure when paired. Ethology, 105(10), 893–908. https://doi.org/10.1046/j.1439-0310.1999.00483.x.
Snowdon, C. T., & Elowson, A. M. (2001). “Babbling” in pygmy marmosets: Development after infancy. Behaviour, 138(10), 1235–1248. https://doi.org/10.1163/15685390152822193.
Snowdon, C. T., & Hodun, A. (1981). Acoustic adaptation in pygmy marmoset contact calls: Locational cues vary with distances between conspecifics. Behavioral Ecology and Sociobiology, 9(4), 295–300. https://doi.org/10.1007/BF00299886.
Soini, P. (1982). Ecology and population dynamics of the pygmy marmoset, Cebuella pygmaea. Folia Primatologica; International Journal of Primatology, 39(1–2), 1–21. https://doi.org/10.1159/000156066.
Tardif, S. D. (2009). The bioenergetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. In N. G. Solomon & J. A. French (Eds.), Cooperative breeding in mammals (pp. 11–33). New York: Cambridge University Press. https://doi.org/10.1017/cbo9780511574634.003.
Tønnessen, M. (2015). The biosemiotic glossary project: Agent, agency. Biosemiotics, 8(1), 125–143. https://doi.org/10.1007/s12304-015-9229-0.
Tucker, A. D., Limpus, C. J., McCallum, H. I., & McDonald, K. R. (1997). Movements and home ranges of Crocodylus johnstoni in the Lynd River, Queensland. Wildlife Research, 24(4), 379–396. https://doi.org/10.1071/WR95073.
von Uexküll, J. (1982). The theory of meaning. Semiotica, 42(1), 25–82. https://doi.org/10.1515/semi.19126.96.36.199.
Wamboldt, M. Z., Gelhard, R. E., & Insel, T. R. (1988). Gender differences in caring for infant Cebuella pygmaea: The role of infant age and relatedness. Developmental Psychobiology, 21(2), 187–202. https://doi.org/10.1002/dev.420210207.
Ward, S. J., & Melfi, V. (2015). Keeper-animal interactions: Differences between the behaviour of zoo animals affect stockmanship. PLoS One, 10(10), 1–10. https://doi.org/10.1371/journal.pone.0140237.
Wells, D. L. (2005). A note on the influence of visitors on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science, 93(1–2), 13–17. https://doi.org/10.1016/j.applanim.2005.06.019.
Wielebnowski, N. C., Fletchall, N., Carlstead, K., Busso, J. M., & Brown, J. L. (2002). Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the north American clouded leopard population. Zoo Biology, 21(1), 77–98. https://doi.org/10.1002/zoo.10005.
We would like to thank Nelly Mäekivi and Masha Kanatova for providing translations for the interview questions in Estonian and Russian and for translating the interview scripts into English. We are also extremely grateful to the Tallinn Zoological Gardens, all the interviewed keepers, and the relevant management for allowing this study.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Cerrone, M. Interspecies Relationships and Their Influence on Animal Handling: a Case Study in the Tallinn Zoological Gardens. Biosemiotics 13, 115–135 (2020). https://doi.org/10.1007/s12304-019-09372-w
- Hybrid environments
- Interspecies communication
- Human-animal relationships