Behavioral enrichment

An Asian elephant in a zoo manipulating a suspended ball provided as environmental enrichment.

Behavioral enrichment (also referred to as environmental enrichment) is an animal husbandry principle that seeks to enhance the quality of captive animal care by identifying and providing the environmental stimuli necessary for optimal psychological and physiological well-being.[1] Environmental enrichment can either be active or passive, depending on whether it requires direct contact between the animal and the enrichment. A variety of enrichment techniques are used to create desired outcomes similar to an animals individual and species' history. Each of the techniques used are intended to stimulate the animal's senses similarly to how they would be activated in the wild. Provided enrichment may be seen in the form of auditory, olfactory, habitat factors, food, research projects, training, and objects.[2]

Purpose

Environmental enrichment improves the overall welfare of animals in captivity and creates a habitat similar to what they would experience in their wild environment. It can aims to maintain an animal's physical and psychological health by increasing the range or number of species-specific behaviors, increasing positive interaction with the captive environment, preventing or reducing the frequency of abnormal behaviors, such as stereotypies, and increasing the individual's ability to cope with the challenges of captivity.[3]

Environmental enrichment can be offered to any animal in captivity, including:

Environmental enrichment can be beneficial to a wide range of vertebrates and invertebrates such as land mammals, marine mammals, and amphibians.[9] In the United States, specific regulations (Animal Welfare Act of 1966) must be followed for enrichment plans in order to guarantee, regulate, and provide appropriate living environments and stimulation for animals in captivity.[10] Moreover, the Association of Zoos and Aquariums (also known as the AZA), requires that animal husbandry and welfare be a main concern for those caring for animals in captivity.

Passive enrichment

Passive enrichment provides sensory stimulation but no direct contact or control. This type of enrichment is commonly used for its potential to benefit several animals simultaneously as well as requiring limited direct animal contact.[11]

Visual enrichment

Visual enrichment is typically provided by changing the layout of an animal's holding area. The type of visual enrichment can vary, from something as simple as adding pictures on walls to videotapes and television. Visual enrichment such as television can especially benefit animals housed in single cages.[12]

Mirrors are also a potential form of enrichment, specifically for animals that display an understanding of self-recognition, such as non-human primates. In addition to using mirrors to reflect the animal's own image, mirrors can also be angled so the animal is able to see normally out-of-sight areas of the holding area.[12]

Enclosures in modern zoos are often designed to facilitate environmental enrichment. For example, the Denver Zoo's exhibit Predator Ridge allows different African carnivores to be rotated among several enclosures, providing the animals with a differently sized environment.

Auditory enrichment

In the wild, animals are exposed to a variety of sounds that they normally do not encounter in captivity. Auditory enrichment can be used to mimic the animal's natural habitat. Types of nature-based auditory enrichment include rainforest sounds and conspecific vocalizations.[12]

The most common form of auditory enrichment is music, whose principal stems primarily from its benefit to humans. The benefits of classical music have been widely studied in animals, from sows[13] to non-human primates.[14] Studies have also looked at various other genres, such as pop and rock, but their ability to provide effective enrichment remains inconclusive.[14][15][16] Most types of music that are selected for enrichment are based on human preferences, causing anthropomorphic biases that may not translate to animals.[16] Therefore, music that is specifically attuned to the animal's auditory senses could be beneficial.[17] Species-specific sounds require further research to find what pitch, frequency, and range is most suitable for the animal.

Active enrichment

Behavioral enrichment – Feeding
Active enrichment during feeding session

Active enrichment often requires the animal to perform some sort of physical activity as well as direct interaction with the enrichment object. Active enrichment items can temporarily reduce stereotypic behaviors as their beneficial effects are usually limited to the short periods of active use.[11]

Behavioral enrichment – Sensory
Inanimate tactile enrichment with paper bag

Inanimate tactile enrichment

Inanimate tactile enrichment encourages the animal to explore and manipulate various kinds of inanimate objects, behaviors that the animal would naturally display in the wild. Most inanimate tactile enrichment occurs in the context of searching for food, such as cracking open a nut or digging holes in tree trunks for worms. Other common manipulable tactile objects include rubber toys stuffed with treats. Instead of providing the food directly, foraging devices are useful in increasing the amount of searching and foraging of food, comparable to the amount of time they would spend in the wild.[12] Elaborate systems of food presentation have also been developed (e.g. presenting dead rats for wildcats in a Swedish zoo) and computer programmed devices which allow the animals in the enclosure to search for prey as they would in their natural environment.

Inanimate tactile enrichment can also be beneficial without the association with food. For example, stones have been shown to encourage exploratory behavior in Japanese macaques. Interaction with the stones exhibited behaviors such as gathering, rolling in hands, rubbing, and carrying.[12]

Other common forms include cardboard, forage, and even the texture of the food (i.e. hard, smooth, cold, warm).[18]

Olfactory enrichment

Olfactory enrichment can stimulate naturalistic behavior, enhance exploration, and reduce inactivity.[19] This type of enrichment is most commonly used for wild felines, both large and small. Exposure to different odors has been shown to influence behavior, resulting in increased activity and exploration.[20] Odors can be smeared or sprayed on an object such as a ball or a tree branch. Types of odors can include catnip, odor of conspecific, or perfume.

Cognitive enrichment

Lack of cognitive stimulation could cause boredom and frustration which are manifested in behavioral disturbances. Because most cognitive enrichment is reinforced with food, it activates reward-related circuits in the brain that can directly affect emotional processes of appraisal.[21] Puzzle feeders are a common method of providing cognitive enrichment, as it makes food harder to access than during routine feeding. Some consider training to be a form of cognitive enrichment, since it requires animals to use their cognitive skills to respond to cues.[22]

Computerized tasks are growing in popularity as it provides feedback as to whether an animal is cognitively enriched. These tasks are designed to test a specific cognitive skill and are standardized so that performance can be compared within and between subjects. It is important to ensure that the task provided is not too easy for the animal, nor too difficult that they get discouraged.[22]

Social enrichment

Social enrichment can either involve housing a group of conspecifics or animals of different species that would naturally encounter each other in the wild. Social animals in particular (i.e. most primates, lions, flamingos, etc.), benefit from social enrichment because it has the positive effect of creating confidence in the group.[23] Social enrichment can encourage social behaviors that are seen in the wild, including feeding, foraging, defense, territoriality, reproduction, and courtship.[24]

Human-interaction enrichment

The most common form of human-interaction enrichment is training. The human and animal interaction during training builds trust, and increases the animal's cooperation during clinical and research procedures. In addition, training sessions have been shown to benefit the welfare of both individually housed animals and communally housed animals by providing cognitive stimulation, increasing social play, decreasing inactivity, and mitigating social aggression during feeding.[25]

Amount of enrichment

A survey of over 200 staff working with mammals at 60 zoos in 13 countries found that all forms of enrichment were considered important for mammals, but several of them were rarely available, because of lack of staff or other priorities.[26]

Type of Enrichment Percent of Staff Ranking This Important or Very Important for Mammals Percent Never Giving This*
Social56%76%
Visual98%75%
Auditory81%74%
Olfactory85%32%
Structural71%28%
Human-animal interaction98%16%
Tactile96%3%
Feeding**41%1%

* time span over a one week period

** feeding enrichment sessions differ from routine feeding sessions

Assessing the success

A range of methods can be used to assess which environmental enrichments should be provided. These are based on the premises that captive animals should perform behaviours in a similar way to those in the ethogram of their ancestral species,[27] animals should be allowed to perform the activities or interactions they prefer, i.e. preference test studies,[28] and animals should be allowed to perform those activities for which they are highly motivated, i.e. motivation studies.[29]

Environmental enrichment is a way to ensure that an animals natural and instinctual behaviors are kept and able to be passed and taught from one generation to the next. Enrichment techniques that encourage species specific behaviors, like those that are discovered in the wild, have been studied and found to help the process of reintroduction of endangered species into their natural habitats, as well as helping to create offspring with natural traits and behaviors.[30]

The main way the success of environmental enrichment can be measured is by recognizing the behavioral changes that occur from the techniques used to shape desired behaviors of the animal compared to the behaviors of those found in the wild.[31] Other ways that the success of environmental enrichment can be assessed quantitatvely by a range of behavioral and physiological indicators of animal welfare. In addition to those listed above, behavioral indicators include the occurrence of abnormal behaviours (e.g. stereotypies,[32][33] cognitive bias studies,[34] and the effects of frustration.[35][36] Physiological indicators include heart rate,[37] corticosteroids,[38] immune function,[39] neuorobiology,[40] eggshell quality[41] and thermography.[42]

It is very difficult for zookeepers to measure the effectiveness of enrichment in terms of the stress due to the fact that animals that are found in zoos are oftentimes on display and presented with very abnormal conditions that can cause uneasiness and stress. Measuring enrichment in terms of reproduction is easier because of our ability to record offspring numbers and fertility. By making necessary environment changes and providing mental stimulation, animals in captivity have been seen to reproduce at a more similar rate to their wild ancestors in comparison to those provided with less behavioral and environmental enrichment.[31]

Issues and concerns

Habituation

Although environmental enrichments can provide sensory and social stimulations, it can also have limited efficacy if not changed frequently. Animals can become habituated to environmental enrichments, showing positive behaviors at onset of exposure and progressively declining with time. Environmental enrichments are effective primarily because it offers novelty stimuli, making the animal's daily routines less predictable, as would be in the wild. Therefore, maintaining novelty is important for the efficacy of the enrichment. Frequently changing the type of environmental enrichment will help prevent habituation.[6]

Training

Usage of more highly advanced enrichment devices, such as computerized devices, requires training. This can lead to issues as training often consists of food as a reward. While food encourages the animal to participate with the device, the animal could associate the device with food. As a result, the interaction with the enrichment would bring about behaviors that are associated with training instead of the desired playful and voluntary behaviors.[43]

Time and resources

The process of producing and providing environmental enrichment usually require a large allocation of time and resources. In a survey,[26] "time taken by animal care staff to complete other tasks" was the most significant factor influencing environmental enrichment provisions and scheduling. Therefore it is important to develop appropriate environmental enrichment programs that can be effectively carried out with the size of staff and time available.

References

  1. ↑ Shepherdson, D.J. (1998) “Tracing the path of environmental enrichment in zoos” in Shepherdson, D.J., Mellen, J.D. and Hutchins, M. (1998) Second Nature – Environmental Enrichment for Captive Animals, 1st Edition, Smithsonian Institution Press, London, UK, pp. 1–12.
  2. ↑ "Animal Enrichment - National Zoo". nationalzoo.si.edu. Retrieved 2016-03-29.
  3. ↑ "Animal Enrichment :: Saint Louis Zoo". www.stlzoo.org. Retrieved 2018-04-11.
  4. ↑ Maple TL (2007). "Toward a science of welfare for animals in the zoo". Journal of Applied Animal Welfare Science. 10 (1): 63–70. doi:10.1080/10888700701277659. PMID 17484680.
  5. ↑ Ron Hines, D.V.M. (2006-04-24). "Synopsis of the Environmental Enrichment Program of 2nd Chance Sanctuary". Archived from the original on 10 June 2006. Retrieved 2006-06-11.
  6. 1 2 Bowman A, Dowell FJ, Evans NP (March 2017). "'The effect of different genres of music on the stress levels of kennelled dogs'". Physiology & Behavior. 171: 207–215. doi:10.1016/j.physbeh.2017.01.024. PMID 28093218.
  7. ↑ Sherwin, C.M. (2007). "Validating refinements to laboratory housing: asking the animals". Retrieved April 9, 2013.
  8. ↑ Hubrecht R (1995). "Dogs and dog housing". In Smith CP, Taylor V. Environmental Enrichment Information Resources for Laboratory Animals. Potters Bar, Herts.: Universities Federation for Animal Welfare (UFAW). pp. 49–62. Archived from the original on 4 April 2002.
  9. ↑ "Alliance of Marine Mammal Parks and Aquariums". www.ammpa.org. Retrieved 2016-03-29.
  10. ↑ Kulpa-Eddy JA, Taylor S, Adams KM (2005-01-01). "USDA perspective on environmental enrichment for animals". ILAR Journal. 46 (2): 83–94. doi:10.1093/ilar.46.2.83. PMID 15775018.
  11. 1 2 Meade TM, Hutchinson E, Krall C, Watson J (September 2014). "Use of an aquarium as a novel enrichment item for singly housed rhesus macaques (Macaca mulatta)". Journal of the American Association for Laboratory Animal Science. 53 (5): 472–7. PMC 4181688. PMID 25255069.
  12. 1 2 3 4 5 Lutz CK, Novak MA (2005). "Environmental enrichment for nonhuman primates: theory and application". ILAR Journal. 46 (2): 178–91. doi:10.1093/ilar.46.2.178. PMID 15775027.
  13. ↑ Silva FR, Miranda KO, Piedade SM, Salgado DD (April 2017). "Effect of Auditory Enrichment (Music) in Pregnant Sows Welfare". Engenharia Agrícola. 37 (2): 215–225. doi:10.1590/1809-4430-eng.agric.v37n2p215-225/2017.
  14. 1 2 Wallace EK, Altschul D, Körfer K, Benti B, Kaeser A, Lambeth S, Waller BM, Slocombe KE (2017-03-29). "Is music enriching for group-housed captive chimpanzees (Pan troglodytes)?". PLOS One. 12 (3): e0172672. doi:10.1371/journal.pone.0172672. PMID 28355212.
  15. ↑ Bowman A, Dowell FJ, Evans NP (March 2017). "'The effect of different genres of music on the stress levels of kennelled dogs'". Physiology & Behavior. 171: 207–215. doi:10.1016/j.physbeh.2017.01.024. PMID 28093218.
  16. 1 2 "Music as enrichment for Sumatran orangutans (Pongo abelii)". Journal of Zoo and Aquarium Research.
  17. ↑ Kędzierski W, Janczarek I, Stachurska A, Wilk I. "Massage or music meant to be relaxing, result in lowering salivary cortisol concentration in race horses". Pferdeheilkunde Equine Medicine. 33 (2): 146–151. doi:10.21836/pem20170206.
  18. ↑ "Enrichment 101: Environment, Enrichment, & Education". www.arkanimals.com. Retrieved 2018-03-28.
  19. ↑ Clark F, King AJ (2008). Chemical Signals in Vertebrates 11. Springer, New York, NY. pp. 391–398. doi:10.1007/978-0-387-73945-8_37. ISBN 9780387739441.
  20. ↑ Wells DL, Egli JM. "The influence of olfactory enrichment on the behaviour of captive black-footed cats, Felis nigripes". Applied Animal Behaviour Science. 85 (1–2): 107–119. doi:10.1016/j.applanim.2003.08.013.
  21. ↑ Meyer S, Puppe B, Langbein J (November 2010). "[Cognitive enrichment in zoo and farm animals--implications for animal behaviour and welfare]". Berliner Und Munchener Tierarztliche Wochenschrift. 123 (11–12): 446–56. PMID 21141273.
  22. 1 2 Clark, Fay. "Cognitive enrichment and welfare: Current approaches and future directions". Animal Behavior and Cognition. 4 (1): 52–71. doi:10.12966/abc.05.02.2017.
  23. ↑ User, Super. "Environmental Enrichment - Colchester Zoo". Retrieved 2018-03-29.
  24. ↑ "Social Enrichment". littlerockzoo.com. Retrieved 2018-03-29.
  25. ↑ Baker KC (May 2004). "Benefits of Positive Human Interaction for Socially-Housed Chimpanzees". Animal Welfare. 13 (2): 239–245. PMC 2875797. PMID 20505791.
  26. 1 2 Hoy JM, Murray PJ, Tribe A (2010). "Thirty years later: enrichment practices for captive mammals" (PDF). Zoo Biology. 29 (3): 303–16. doi:10.1002/zoo.20254. PMID 19434736.
  27. ↑ Dawkins MS (1989). "Time budgets in red junglefowl as a baseline for the assessment of welfare in domestic-fowl". Applied Animal Behaviour Science. 24: 77–80. doi:10.1016/0168-1591(89)90126-3.
  28. ↑ Sherwin CM, Glen EF (2003). "Cage colour preferences and effects of home-cage colour on anxiety in laboratory mice". Animal Behaviour. 66: 1085–1092.
  29. ↑ Sherwin CM (2004). "The motivation of group-housed laboratory mice, Mus musculus, for additional space". Animal Behaviour. 67: 711–717. doi:10.1016/j.anbehav.2003.08.018.
  30. ↑ Shepherdson O (1994-01-01). Olney PJ, Mace GM, Feistner AT, eds. The role of environmental enrichment in the captive breeding and reintroduction of endangered species. Springer Netherlands. pp. 167–177. doi:10.1007/978-94-011-0721-1_8. ISBN 9789401043113.
  31. 1 2 Moberg GP, Mench JA (2000-01-01). The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. CABI. ISBN 9780851999302.
  32. ↑ Mason GJ (1991). "Stereotypies - A critical review". Animal Behaviour. 41: 1015–1037. doi:10.1016/S0003-3472(05)80640-2.
  33. ↑ Claes A, Attur Shanmugam A, Jensen P (2010). "Habituation to environmental enrichment in captive Sloth Bears-effect on stereotypies". Zoo Biology. 29: 705–714. doi:10.1002/zoo.2030.
  34. ↑ Mendl M, Burman OH, Parker RM, Paul ES (2009). "Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms". Applied Animal Behaviour Science. 118: 161–181.
  35. ↑ Duncan IJ, Wood-Gush DG (1971). "Frustration and aggression in the domestic fowl". Animal Behaviour. 19: 500–504.
  36. ↑ Zimmerman PH, Lundberg A, Keeling LJ, Koene P (2003). "The effect of an audience on the gakel-call and other frustration behaviours in the laying hen (Gallus gallus domesticus)". Animal Welfare. 12: 315–326.
  37. ↑ Kemppinen N, Hau J, Meller A, Mauranen K, Kohila T, Nevalainen T (2010). "Impact of aspen furniture and restricted feeding on activity, blood pressure, heart rate and faecal corticosterone and immunoglobulin A excretion in rats (Rattus norvegicus) housed in individually ventilated cages". Laboratory Animals. 44: 104–112.
  38. ↑ Laws N, Ganswindt A, Heistermann M, Harris M, Harris S, Sherwin C (2007). "A case study: fecal corticosteroid and behavior as indicators of welfare during relocation of an asian elephant". Journal of Applied Animal Welfare Science. 10: 349–358. doi:10.1080/10888700701555600.
  39. ↑ Martin LB, Kidd L, Liebl AL, Coon CA (August 2011). "Captivity induces hyper-inflammation in the house sparrow (Passer domesticus)". The Journal of Experimental Biology. 214 (Pt 15): 2579–85. doi:10.1242/jeb.057216. PMID 21753052.
  40. ↑ Lewis MH, Presti MF, Lewis JB, Turner CA (2006). "The neurobiology of stereotypy I: Environmental complexity.". In Mason G, Rushen J. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare. CABI. pp. 190–226. doi:10.1079/9780851990040.0190.
  41. ↑ Hughes BO, Gilbert AB, Brown MF (1986). "Categorisation and causes of abnormal egg shells: relationship with stress". British Poultry Science. 27: 325–337.
  42. ↑ Wilcox CS, Patterson J, Cheng HW (2009). "bumblefoot". Poultry Science. 88: 1176–1180. doi:10.3382/ps.2008-00446.
  43. ↑ French F, Mancini C, Sharp H (April 2018). "High tech cognitive and acoustic enrichment for captive elephants". Journal of Neuroscience Methods. 300: 173–183. doi:10.1016/j.jneumeth.2017.09.009. PMID 28951175.
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