Behavioral 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 animal's 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]

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

Purpose

Environmental enrichment can improve the overall welfare of animals in captivity and create a habitat similar to what they would experience in their wild environment. It 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] Stereotypies are seen in captive animals due to stress and boredom. This includes pacing, self-harm, over-grooming, head-weaving, etc.[4]

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.[10] 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.[11] 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.[12]

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.[13]

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.[13]

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 rain forest sounds and con-specific vocalizations.[13]

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[14] to non-human primates.[15] Studies have also looked at various other genres, such as pop and rock, but their ability to provide effective enrichment remains inconclusive.[15][16][17] Most types of music that are selected for enrichment are based on human preferences, causing anthropomorphic biases that may not translate to animals.[17] Therefore, music that is specifically attuned to the animal's auditory senses could be beneficial.[18] Species-specific sounds require further research to find what pitch, frequency, and range is most suitable for the animal.

Active enrichment

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.[12]

Inanimate tactile enrichment with paper bag

Food-based enrichment

Food-based enrichment is meant to mimic what a captive animal would do in the wild for food. This is extremely important because in the wild, animals are adapted to work hard for what they eat. A lot of time and energy is spent finding food, which is why this tactic is used to make it more challenging for the animal rather than just feeding it simple food.[19] Forcing the animal to work for its food causes more stimulation, preventing it from becoming bored.[19] This kind of enrichment can also help with a captive animal's physical health because it could force the animal to be more active.[19] For example, food can be hidden and spread cross an enclosure making the animal actively search for it. 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.[13] Most food-based enrichment occurs in the context of searching for food, such as cracking open a nut or digging holes in tree trunks for worms.

Structural enrichment

A structure built for baboons at the Oakland Zoo

Structural Enrichment is when objects are added to an enclosure to mimic an animal’s natural habitat. These objects can be switched out occasionally or kept permanently.[20] The environment of captive animals should be switched frequently since their environment in the wild would bring on new objects and exploration. The animal should never become too familiar with their environment because that can cause boredom, no stimulation or stereotypical behavior.[20] Examples of this could be swings or climbing structures.[20] Stones have also been shown to encourage exploratory behavior in Japanese macaques. Interaction with the stones exhibited behaviors such as gathering, rolling in hands, rubbing, and carrying.[13]

Other common forms include cardboard, forage, and even the texture of the food (i.e. hard, smooth, cold, warm).[21]

Olfactory enrichment

Olfactory enrichment can stimulate naturalistic behavior, enhance exploration, and reduce inactivity.[22] 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.[23] 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

In the wild, animals deal with ecological challenges in order to acquire the resources, such as food and shelter, that they require to survive.[24] These challenges arise from interactions with other animals, or through changes to their environment that require the individuals to exercise their cognitive ability and to improve their behavioral strategies.[24] Therefore, these challenges act as an important problem-solving element in the animals' day-to-day lives, and in-turn, increases their overall fitness.[24] Lack of cognitive stimulation can cause boredom and frustration which can potentially lead to abnormal behaviors.[25]

Cognitive enrichment has been gaining more attention in the last few decades as it has shed some light on the importance of ecological challenges for captive animals, specifically laboratory, farm and zoo, as a means for improving wellbeing.[26] However, there is no current consensus on the definition of this term.[26] A proposed definition of cognitive enrichment is as follows: improving animal welfare by providing opportunities for captive animals to use cognitive skills for problem solving and providing limited control over some aspects of its environment.[27] Typically, it involves a reward, be it a sense of satisfaction or receiving something tangible such as food.[26] The animal therefore anticipates positive benefits from a challenging situation[28] which can directly affect its emotional processes.[25] Cognitive enrichment should be provided in addition to a diverse environment that is already structurally and socially enriched; it goes beyond the basic needs of the animals.[28]

Cognitive enrichment can, however, overlap with other categories of enrichment.[29] For instance, puzzle feeders are becoming a common practice, providing more challenge and skill than a routine feeding.[26] Providing new toys in the environment and increasing social opportunities for rodents also increase cognitive stimulation.[30] Some also consider training to be a form of cognitive enrichment, as it requires animals to use their cognitive skills to perform tasks in response to specific cues.[26]

The term ‘cognitive enrichment’ first emerged in a 2003 study on age-dependent cognition in beagle dogs.[31] The study found that given enough time, older animals still had the capacity to improve their cognitive skills.[31] Research has also shown that more cognitive enrichment earlier in life affects long-term cognitive performance.[29]

Laboratory research has demonstrated that increased cognitive enrichment can potentially improve laboratory sanitation, and the health and wellbeing of the animals.[32] For example, one experiment used clicker training as positive reinforcement with laboratory mice in a three-week session with three different training challenges.[32] Consequently, the trained mice exhibited a decreased fear of humans, depressive behaviors, and vocalizations.[32]

Research on long-term cognitive enrichment in farm animals has also been tested using domestic pigs.[33] The experiment began by conditioning the pigs to respond to unique acoustic noises in order to receive their food.[33] Once they knew their own sound, they would be summoned individually to the feeding area.[33] In the next phase, the pigs were required to press a button in order to receive their food and the number of times they needed to press the button increased with time.[33] The pigs in the experiment that performed the cognitive enrichment were significantly less aggressive than the control pigs, experienced positive physiological changes, and were less fearful and more exploratory in novel situations.[33]

Relative to the laboratory and farm setting, it appears that there are a limited number of research articles that have tested cognitive enrichment in zoos with definitive and measurable results. In a review of enrichment in nonhuman primate captivity, there were some mixed conclusions.[34] It was found the puzzle box feeders increased foraging time for various species, a behavior which can be correlated with a decrease in aggressive and abnormal behaviors.[34] However, in some cases there were no observable changes in its effects,[35] and even an increase in aggression over competition for the puzzle box.[34] There is evidence of a successful cognitive enrichment technique in one zoo where the chimpanzees were required to use various tools in feeder contraptions in order to replicate potential instances in their natural environment.[36] The study was set up with different levels so they could slowly learn the techniques, so as to not discourage the chimpanzees.[36] These specially designed feeders increased tool-using behaviors, while reducing abnormal and self-directed behaviors.[36] The authors, however, do admit there were not many abnormal behaviors to begin with from this small sample group (n=5).[36] Research has found that there is a need for additional cognitive enrichment in aquariums for cetaceans and pinnipeds that goes beyond animal training.[37] Examples include encouraging increased choice, allowing additional control over their environment, and promoting more under-water problem solving devices and tasks.[37]

Computerized and touchscreen tasks are growing in popularity as they provide feedback as to whether an animal is being cognitively stimulated, whether the task is overly challenging (potentially causing frustration) or not challenging enough (potentially causing boredom).[26] These challenges typically test a specific cognitive skill and are designed so that results can be compared between individuals.[26] However, it has been said that computerized tasks are not ideal or practical for a zoo enclosure setting.[35]

Animal welfare research has been criticized for being anthropocentric, emotionally driven rather than scientific.[38] It is argued that there is a need to take an allostasis view (stability through change), instead of a homeostasis view (maintained at a set point) of animal wellbeing[38] which could potentially be achieved through improved cognitive enrichment. It is also argued that the success of enrichment is too often measured by observing a decrease in negative behaviour, for instance aggression, and that it should be measured by indication of good wellbeing and positive emotion.[28] Others emphasize that it is crucial that there be benefits to the animal’s welfare in order for the process to be considered cognitive enrichment.[37]

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.[39] Social enrichment can encourage social behaviors that are seen in the wild, including feeding, foraging, defense, territoriality, reproduction, and courtship.[40]

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.[41]

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.[42]

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 enrichment should be provided. These are based on the premises that captive animals should perform behaviors in a similar way to those in the ethogram of their ancestral species,[43] animals should be allowed to perform the activities or interactions they prefer, i.e. preference test studies,[44] and animals should be allowed to perform those activities for which they are highly motivated, i.e. motivation studies.[45]

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.[46]

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.[47] Other ways that the success of environmental enrichment can be assessed quantitatively 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,[48][49] cognitive bias studies,[50] and the effects of frustration.[51][52] Physiological indicators include heart rate,[53] corticosteroids,[54] immune function,[55] neuorobiology,[56] eggshell quality[57] and thermography.[58]

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.[47]

Issues and concerns

Habituation

Although environmental enrichment 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.[7]

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.[59]

Time and resources

The process of producing and providing environmental enrichment usually require a large allocation of time and resources. In a survey,[42] "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. Archived from the original on 2016-04-01. Retrieved 2016-03-29.
  3. "Animal Enrichment :: Saint Louis Zoo". www.stlzoo.org. Retrieved 2018-04-11.
  4. "Towards an Understanding of Stereotypic Behaviour in Laboratory Macaques". awionline.org. Retrieved 2019-02-27.
  5. Maple TL (2007). "Toward a science of welfare for animals in the zoo". Journal of Applied Animal Welfare Science. 10 (1): 63–70. CiteSeerX 10.1.1.560.8948. doi:10.1080/10888700701277659. PMID 17484680. S2CID 32358898.
  6. 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.
  7. Bowman A, Dowell FJ, Evans NP (March 2017). "The effect of different genres of music on the stress levels of kennelled dogs" (PDF). Physiology & Behavior. 171: 207–215. doi:10.1016/j.physbeh.2017.01.024. PMID 28093218. S2CID 207377805.
  8. Sherwin, C.M. (2007). "Validating refinements to laboratory housing: asking the animals". Retrieved April 9, 2013.
  9. Hubrecht R (1995). "Dogs and dog housing". In Smith CP, Taylor V (eds.). 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.
  10. "Alliance of Marine Mammal Parks and Aquariums". www.ammpa.org. Archived from the original on 2016-03-29. Retrieved 2016-03-29.
  11. 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.
  12. 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.
  13. 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.
  14. 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.
  15. 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. Bibcode:2017PLoSO..1272672W. doi:10.1371/journal.pone.0172672. PMC 5371285. PMID 28355212.
  16. Bowman A, Dowell FJ, Evans NP (March 2017). "The effect of different genres of music on the stress levels of kennelled dogs" (PDF). Physiology & Behavior. 171: 207–215. doi:10.1016/j.physbeh.2017.01.024. PMID 28093218. S2CID 207377805.
  17. Ritvo, Sarah E.; MacDonald, Suzanne E. (2016). "Music as enrichment for Sumatran orangutans (Pongo abelii)". Journal of Zoo and Aquarium Research. 4 (3). doi:10.19227/jzar.v4i3.231.
  18. Kędzierski W, Janczarek I, Stachurska A, Wilk I (2017). "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.
  19. Orangutan Project (2015). "Orangutan Project Enrichment" (PDF). Cite journal requires |journal= (help)
  20. Orangutan Project (2015). "Orangutan Project Enrichment" (PDF). Cite journal requires |journal= (help)
  21. "Enrichment 101: Environment, Enrichment, & Education". www.arkanimals.com. Retrieved 2018-03-28.
  22. 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.
  23. Wells DL, Egli JM (2004). "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.
  24. Meehan, Cheryl L.; Mench, Joy A. (February 2007). "The challenge of challenge: Can problem solving opportunities enhance animal welfare?". Applied Animal Behaviour Science. 102 (3–4): 246–261. doi:10.1016/j.applanim.2006.05.031.
  25. Meyer, Susann; Puppe, Birger; Langbein, Jan (November 2010). "[Cognitive enrichment in zoo and farm animals--implications for animal behaviour and welfare]". Berliner und Munchener Tierarztliche Wochenschrift. 123 (11–12): 446–456. ISSN 0005-9366. PMID 21141273.
  26. Clark, Fay (2017-02-01). "Cognitive enrichment and welfare: Current approaches and future directions". Animal Behavior and Cognition. 4 (1): 52–71. doi:10.12966/abc.05.02.2017.
  27. Clark, Fay E. (November 2011). "Great ape cognition and captive care: Can cognitive challenges enhance well-being?". Applied Animal Behaviour Science. 135 (1–2): 1–12. doi:10.1016/j.applanim.2011.10.010.
  28. Boissy, Alain; Manteuffel, Gerhard; Jensen, Margit Bak; Moe, Randi Oppermann; Spruijt, Berry; Keeling, Linda J.; Winckler, Christoph; Forkman, Björn; Dimitrov, Ivan; Langbein, Jan; Bakken, Morten (October 2007). "Assessment of positive emotions in animals to improve their welfare". Physiology & Behavior. 92 (3): 375–397. doi:10.1016/j.physbeh.2007.02.003. PMID 17428510. S2CID 10730923.
  29. Milgram, Norton W.; Siwak-Tapp, Christina T.; Araujo, Joseph; Head, Elizabeth (August 2006). "Neuroprotective effects of cognitive enrichment". Ageing Research Reviews. 5 (3): 354–369. doi:10.1016/j.arr.2006.04.004. PMID 16949888. S2CID 44926548.
  30. Lambert, Talley J.; Fernandez, Stephanie M.; Frick, Karyn M. (May 2005). "Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice". Neurobiology of Learning and Memory. 83 (3): 206–216. doi:10.1016/j.nlm.2004.12.001. PMID 15820856. S2CID 6130770.
  31. Milgram, Norton W. (2003-11-01). "Cognitive Experience and Its Effect on Age-Dependent Cognitive Decline in Beagle Dogs". Neurochemical Research. 28 (11): 1677–1682. doi:10.1023/A:1026009005108. ISSN 1573-6903. PMID 14584821. S2CID 10641853.
  32. Leidinger, Charlotte; Herrmann, Felix; Thöne-Reineke, Christa; Baumgart, Nadine; Baumgart, Jan (2017-03-06). "Introducing Clicker Training as a Cognitive Enrichment for Laboratory Mice". Journal of Visualized Experiments (121): 55415. doi:10.3791/55415. ISSN 1940-087X. PMC 5408971. PMID 28287586.
  33. Zebunke, Manuela; Puppe, Birger; Langbein, Jan (June 2013). "Effects of cognitive enrichment on behavioural and physiological reactions of pigs". Physiology & Behavior. 118: 70–79. doi:10.1016/j.physbeh.2013.05.005. PMID 23680428. S2CID 10751502.
  34. Honess, P.E.; Marin, C.M. (January 2006). "Enrichment and aggression in primates". Neuroscience & Biobehavioral Reviews. 30 (3): 413–436. doi:10.1016/j.neubiorev.2005.05.002. PMID 16055188. S2CID 33130527.
  35. Clark, Fay E.; Gray, Stuart I.; Bennett, Peter; Mason, Lucy J.; Burgess, Katy V. (2019-07-09). "High-Tech and Tactile: Cognitive Enrichment for Zoo-Housed Gorillas". Frontiers in Psychology. 10: 1574. doi:10.3389/fpsyg.2019.01574. ISSN 1664-1078. PMC 6629937. PMID 31354581.
  36. Yamanashi, Yumi; Matsunaga, Masayuki; Shimada, Kanae; Kado, Ryuichiro; Tanaka, Masayuki (2016-08-02). "Introducing tool-based feeders to zoo-housed chimpanzees as a cognitive challenge: spontaneous acquisition of new types of tool use and effects on behaviours and use of space". Journal of Zoo and Aquarium Research. 4 (3). doi:10.19227/jzar.v4i3.235. ISSN 2214-7594.
  37. Clark, Fay E. (2013-07-24). "Marine mammal cognition and captive care: A proposal for cognitive enrichment in zoos and aquariums". Journal of Zoo and Aquarium Research. 1 (1): 1–6. doi:10.19227/jzar.v1i1.19. ISSN 2214-7594.
  38. Korte, S. Mechiel; Olivier, Berend; Koolhaas, Jaap M. (October 2007). "A new animal welfare concept based on allostasis" (PDF). Physiology & Behavior. 92 (3): 422–428. doi:10.1016/j.physbeh.2006.10.018. PMID 17174361. S2CID 14815077.
  39. User, Super. "Environmental Enrichment - Colchester Zoo". Retrieved 2018-03-29.
  40. "Social Enrichment". littlerockzoo.com. Archived from the original on 2018-04-12. Retrieved 2018-03-29.
  41. Baker KC (May 2004). "Benefits of Positive Human Interaction for Socially-Housed Chimpanzees". Animal Welfare. 13 (2): 239–245. PMC 2875797. PMID 20505791.
  42. Hoy JM, Murray PJ, Tribe A (2010). "Thirty years later: enrichment practices for captive mammals". Zoo Biology. 29 (3): 303–16. doi:10.1002/zoo.20254. PMID 19434736.
  43. 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.
  44. Sherwin CM, Glen EF (2003). "Cage colour preferences and effects of home-cage colour on anxiety in laboratory mice". Animal Behaviour. 66 (6): 1085–1092. doi:10.1006/anbe.2003.2286. S2CID 53191108.
  45. Sherwin CM (2004). "The motivation of group-housed laboratory mice, Mus musculus, for additional space". Animal Behaviour. 67 (4): 711–717. doi:10.1016/j.anbehav.2003.08.018. S2CID 53181481.
  46. Shepherdson O (1994-01-01). "The role of environmental enrichment in the captive breeding and reintroduction of endangered species". In Olney PJ, Mace GM, Feistner AT (eds.). Creative Conservation. Springer Netherlands. pp. 167–177. doi:10.1007/978-94-011-0721-1_8. ISBN 9789401043113.
  47. Moberg GP, Mench JA (2000-01-01). The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. CABI. ISBN 9780851999302.
  48. Mason GJ (1991). "Stereotypies - A critical review". Animal Behaviour. 41 (6): 1015–1037. doi:10.1016/S0003-3472(05)80640-2. hdl:10214/4622. S2CID 53187334.
  49. Claes A, Attur Shanmugam A, Jensen P (2010). "Habituation to environmental enrichment in captive Sloth Bears—effect on stereotypies". Zoo Biology. 29 (6): 705–714. doi:10.1002/zoo.20301. PMID 20069629.
  50. 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 (3–4): 161–181. doi:10.1016/j.applanim.2009.02.023.
  51. Duncan IJ, Wood-Gush DG (1971). "Frustration and aggression in the domestic fowl". Animal Behaviour. 19 (3): 500–504. doi:10.1016/S0003-3472(71)80104-5. PMID 5167834.
  52. 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.
  53. 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 (2): 104–112. doi:10.1258/la.2009.009058. PMID 19854757. S2CID 17743686.
  54. 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 (4): 349–358. doi:10.1080/10888700701555600. PMID 17970634. S2CID 46617133.
  55. 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. S2CID 31326602.
  56. Lewis MH, Presti MF, Lewis JB, Turner CA (2006). "The neurobiology of stereotypy I: Environmental complexity.". In Mason G, Rushen J (eds.). Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare. CABI. pp. 190–226. doi:10.1079/9780851990040.0190. ISBN 9780851990040.
  57. Hughes BO, Gilbert AB, Brown MF (1986). "Categorisation and causes of abnormal egg shells: relationship with stress". British Poultry Science. 27 (2): 325–337. doi:10.1080/00071668608416885. PMID 3742268.
  58. Wilcox CS, Patterson J, Cheng HW (2009). "Use of thermography to screen for subclinical bumblefoot in poultry". Poultry Science. 88 (6): 1176–1180. doi:10.3382/ps.2008-00446. PMID 19439627.
  59. French F, Mancini C, Sharp H (April 2018). "High tech cognitive and acoustic enrichment for captive elephants" (PDF). Journal of Neuroscience Methods. 300: 173–183. doi:10.1016/j.jneumeth.2017.09.009. PMID 28951175. S2CID 4548453.
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