The effect of auditory enrichment, rearing method and social environment on the behavior of zoo-housed psittacines (Aves: Psittaciformes); implications for welfare

https://doi.org/10.1016/j.applanim.2016.10.013Get rights and content

Highlights

  • Zoo housed psittacines exposed to different types of auditory stimulation showed differences in behaviour.

  • Exposure to talking radio and pop music significantly reduced psittacine vocalisation.

  • Hand-reared birds showed more stereotypy and interacted less with enrichment than parent-reared.

  • Solo-housed birds showed more stereotypy than group housed birds.

  • Solo-housed, hand-reared birds may be at risk of reduced welfare in zoo settings.

Abstract

The psychological and physiological effects of different genres of music are well documented in humans. These concepts have also been studied in kenneled dogs and some exotic animals, implying that animals may experience benefits similar to those of humans. This study tested the hypothesis that auditory enrichment changed the behavior of ten zoo-housed psittacines. All animals were exposed to six conditions of auditory stimulation; a ‘control’ (no auditory stimulation), and ‘experimental’ conditions, during which animals were presented with commercially-available CDs of classical music, pop music, natural rainforest sounds, parrot sounds and a talking radio. Each type of stimulation lasted two days, with a wash-out day between different stimulation conditions. We recorded key parameters relating to the birds’ social environment – whether they were group or single-housed and whether they had been hand or parent-reared. The parrots’ behaviour was recorded every minute for a 25 min period seven times a day using instantaneous sampling. The incidence of calm vocalisations and the level of preening changed with the different conditions. Birds exposed to rainforest and talking radio preened more than control birds. Birds exposed to several genres of auditory stimulation expressed fewer calm vocalisations than control birds. A further finding from this study was that hand-reared birds exhibited dramatically increased incidences of stereotypic behavior, more learned vocalisation and interacted less with enrichment than parent-reared and the implications of hand rearing for welfare are discussed. Similarly solo housed birds showed changes in behavior compared to group housed, such as less preening and more stereotypic behaviour. Hand reared, solo housed parrots express less normal behavior and maybe at risk of impaired welfare.

Introduction

Millions of animals are kept in captivity globally, in zoos, laboratories, safari parks and animal shelters with millions more kept as pets (Wells, 2009). Parrots are the third most popular companion animal in the USA with estimated figures of 10 million individuals being kept as pets (Van Hoek and Cate, 1998, Kalmar et al., 2010). Unlike many companion animals, parrots are only in the very early stages of domestication and are genetically similar to their wild ancestors, so their ethological needs in captivity are complex and relatively unchanged from those in the wild (Meehan et al., 2003a, Meehan et al., 2003b, Meehan et al., 2003c). Recently there has been an increased interest in the study of parrot intelligence, behaviour, and welfare (Engebretson, 2006, Pepperberg, 2006, Speer, 2014). In the wild animals are exposed to an ever-changing physical, social and sensory environment and one of the greatest challenges of keeping animals in captive conditions is providing enrichment that allows captive animals to engage in behaviour that satisfies their ethological requirements (Shepherdson et al., 2012). As a result of lack of appropriate behavioural opportunities or choices abnormal behaviours including stereotypies can occur (Mason, 1991), which are believed to be indicative of poor welfare. Stereotypic behaviour can be defined as a repetitive, unvarying and apparently functionless behaviour pattern which is rarely, if at all seen in the wild (Mason, 1991, Cooper and Nicol, 1996, Mason et al., 2007). Psittacines are particularly vulnerable to stereotypy (Van Hoek and Cate, 1998) which can include feather plucking, screaming, self-mutilation and, when all coping mechanisms fail, learned helplessness (Wilson, 2001, Garner et al., 2003, Mason et al., 2007, Van Zeeland et al., 2009). Concerns about abnormal and stereotypic behaviour displayed in captive animals have resulted in the development of environmental enrichment to allow animals to express more natural behaviour (Swaisgood and Shepherdson, 2005). Environmental enrichment is a common term used for improving the captive environment of animals and can be broadly defined as any technique used to improve the biological functioning and welfare of a captive animal through modifications of its environment (Newberry, 1995). It is thought that enrichment is a useful way to eliminate abnormal behaviours and improve animal welfare, if used in combination with other improvements in housing and husbandry (Mason et al., 2007).

To date, there are only a limited number of studies that have explored the effect of environmental enrichment on the behaviour and welfare of captive psittacines. Studies have focused on enclosure design and size (Mettke-Hofmann et al., 2002; Meehan et al., 2004) and enrichment through social and physical modifications (Meehan et al., 2003a, Meehan et al., 2003b, Meehan et al., 2003c, Van Hoek and Cate, 1998, Kalmar et al., 2010, Kim et al., 2009). Findings from these studies showed that parrots without access to enrichment developed significantly more stereotypy than those that lived in enriched environments (Meehan et al., 2004).

The value of auditory stimulation for psychological well-being has been documented in humans (Maratos et al., 2008, Gold et al., 2009). It has been suggested that the moods (McCraty et al., 1998) and behaviour (Yalch and Spangenberg, 2000) of humans can be strongly influenced by the type of auditory stimulation to which they are exposed (Wells, 2009). For example, rock music can result in increased sadness, tension and fatigue, whilst “designer music” (music which is created to have a specific effect on the listener) results in relaxation (Wells, 2009). These results have led to research on the use of auditory stimulation for animal enrichment. Not only can auditory stimulation provide enrichment benefits but can also serve as a tool to mask potentially aversive noise and negative acoustic stimuli such as the sound of machinery (Wells, 2009).The value of music for improving welfare has been reported in animals (Kaplan, 2009) including non-human primates (Shepherdson et al., 1989), African leopard (Panthera pardus pardus) (Markowitz et al., 1995, Tromborg et al., 1993), chickens (Gallus gallus domesticus) (Gvaryahu et al., 1989) and kenneled dogs (Canis lupus familaris) (Boone and Quelch, 2003). Many of these studies reported positive changes in the behaviour or physiology of the animals exposed to auditory stimulation which included ecologically-relevant sounds, classical music and radio broadcasts. Examples of the effects of enrichment included reduced respiratory rate in dogs (Wells et al., 2002), improved growth rate of chickens (Gvaryahu et al., 1989) and reduced incidences of abnormal behaviour including stereotypy and enhanced general well-being in Asian elephants (Wells and Irwin, 2008) and African Leopards (Markowitz et al., 1995). Although birds have been shown to appreciate and respond to music (Kaplan, 2009) to our knowledge, there have been no studies to date on the effectiveness of auditory enrichment for psittacines. This study aimed to determine whether different types of auditory stimulation had an effect on psittacine behavior.

Rearing method is known to have an effect on the behaviour and welfare of psittacines (Luescher and Shannon, 2005) as hand rearing involves separating the psittacine chick from its parents, thereby depriving the bird of contact which allows normal social and sexual development (Fox, 2006). Hand reared birds are often imprinted socially and sexually onto humans, leading them to prefer contact with humans over that of conspecifics (Fox, 2006). Thus, hand rearing has the potential to compromise welfare and has been banned in some EU countries, such as the Netherlands. Hand rearing is becoming increasingly popular to satisfy demand for tame birds from the pet trade (Schmid et al., 2006) so we also considered the effects of hand rearing vs parent rearing on the behaviour of the birds. As wild psittacines are highly social, isolation may be a welfare risk so we also looked at the effect of paired and single housing on several categories of behavior.

Section snippets

Subjects

A total of ten individuals were observed during this study, 1:0 yellow-headed amazon parrot (Amazona oratrix), 1:1 African grey parrot (Psittacus erithacus), 0:1 hyacinth macaw (Anodorhynchus hyacinthinus), 2:0 scarlet macaw (Ara macao), 0:2 military macaw (Ara militaris), 1:1 blue and gold macaw (Ara ararauna). Although the parrots were of several species, most parrot species have broadly similar behaviour and ethological needs (Meehan and Mench, 2006, Seibert, 2006). Birds were aged between 3

Auditory enrichment

For the various categories of behaviour studied, only preening behavior and calm vocalisation showed significant differences between groups (Table 2).

For calm vocalization (Fig. 1) the following conditions were significantly different from control (using a significance level of 0.01 after correction for multiple testing): pop v control (paired t-test; n = 10; p = 0.0034) and talking radio v control (paired t-test; n = 10; p = 0.0034). Talking radio and pop music reduced the level of calm vocalization

Discussion

Psittacines in captivity are highly prone to stereotypic patterns of behaviour, often thought to be caused by factors including lack of social interaction with other psittacines and housing conditions (Garner et al., 2006). The most common stereotypic behaviour displayed in parrots includes feather plucking (Van Zeeland et al., 2009), followed by biting and screaming (Wilson, 2001), although at Whipsnade Zoo bar biting was the most prevalent. Some handlers and owners consider stereotypic

Conclusion

Overall, this study suggests that captive parrots’ behaviour can be influenced by their auditory environment, as well as their social grouping and their rearing history. However, this study was conducted on a small number of animals over a short period of time. Therefore, further research is necessary to determine the long-term effects of auditory stimulation using a larger sample size before generalized conclusions can be confirmed. The results also show that single housing and hand rearing

Acknowledgements

The authors wish to thank the flying birds team at ZSL Whipsnade Zoo for allowing observation of their parrots and Anglia Ruskin University where the authors formerly worked/studied. The authors are grateful to two anonymous reviewers whose comments greatly improved the manuscript.

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