S16.3: Environmental enrichment and bird welfare

Multifarious definitions for the term ‘welfare’ exist, as discussed in diverse publications (e.g. Dawkins 1990; Duncan & Poole 1990; Barnard & Hurst 1996; Fraser et al. 1997; Robinson 1998). Fraser et al. (1997) found that definitions of welfare are generally framed in one or more of three concerns: the feelings or emotions of the animal, its possibilities for natural living or the functioning of its biological systems. They contend that only the combination of all three classes of problems together cover the quality-of-life concerns on which animal welfare research is based. I think that this is a very realistic assessment.

The term ‘enrichment’ is also varied in its usage. It is usually qualified adjectivally, for example as environmental-, habitat- or behavioural- enrichment. Enriching in these contexts generally means the addition of components that lead to an increase in complexity (Robinson 1998). The working definition of (environmental) enrichment used at Rotterdam Zoo is ‘elements in the enclosure of an animal that enable it to carry out natural activity patterns’. Activity patterns can occur in various forms of periodicity, for example in circadian, seasonal or annual cycles. Elements can be physical structures integral to the enclosure design, food/objects placed temporarily in the enclosure or other non-object stimuli. A broad interpretation includes presence of con- or heterospecifics.

Welfare and environmental enrichment considerations are somewhat different for the three primary categories of captive birds, i.e. zoo, farm and cage birds. The emphasis in the zoo approach is in provision of an environment that permits animals to explore and allows them to perform most of the behaviours in their natural repertoire. This is not only for welfare reasons, but also because it increases the attractiveness of the animals to people, enabling zoos to carry out their essential conservation education task more effectively (IUDZG/CBSG (IUCN/SSC) 1993; Robinson 1998). Zoo enrichment efforts also often have the goal of increasing multidimensional enclosure use, i.e. to increase the effectiveness of use of the space provided to enclosure inhabitants.

The stimulus that elicits a natural behaviour need not be natural, but rather may serve as a functional replacement to a natural stimulus. However there is increasing pressure for zoos to use only enrichment elements that are visually compatible with the habitat ‘immersion’ concept currently embraced by zoos. The immersion concept involves the creation of illusions that involve zoo visitors in the environmental circumstances of the animal (IUDZG/CBSG (IUCN/SSC) 1993). Thus non-natural appearing elements that would detract from an illusion are often excluded from use, regardless of their suitability (Robinson 1998).

Environmental enrichment efforts for farm animals, e.g. poultry, focus on alleviating or preventing abnormal behaviours or otherwise improving welfare without sacrificing production and profit. Public perception of welfare needs is also of relevance with farm animals; Appleby (1993) cites an example in which public concern about welfare relative to housing of laying hens resulted in legislation actually detrimental to the welfare of the hens. However, the concern about the ‘naturalness’ of elements employed to enrich the animals in zoos is not similarly applied to farm animals (Robinson 1998). Little is known about the functionality and causation of abnormal behaviours commonly observed in farm birds. For example, despite the seriousness of feather picking problems leading to feather damage, injuries and even mortality in domestic fowl, there is no consensus as whether these problems are related to dustbathing or foraging (Vestergaard 1994; Huber-Eicher & Wechsler 1997).

Management of cage birds (usually pet song birds and parrots), is often guided by practical and aesthetic factors. Studies of abnormal behaviour, and application of enrichment efforts are few, and most information in these areas is largely anecdotal (van Hoek 1995).

The zoo enrichment concept, i.e. all animals should be provided with an environment that allows them to perform most of the behaviours in their natural repertoire, implies that the welfare (not to mention the educational-exhibit value) of the animal is compromised by non-performance of the behaviours. This position is thus immune to subjective assessments of the degree to which an animals welfare is compromised by not having opportunities to perform such behaviours.

Such subjective assessment can lead to misguided prioritisation of enrichment efforts. In an argument that behavioural needs of mammals exceeds that of other animals and that enrichment efforts should be allocated accordingly Poole (1992) states that ‘A toad may need to have moving prey, a fish facilitates to build a nest, a reptile a facility to sun itself or a bird the opportunity to dust bathe. Satisfying these ethological needs releases a sequence of innate behaviours, but there is no evidence that absence of an appropriate facility compromises the individual's well-being’. Contrarily, in the same volume, van Liere (1992) found that ‘a chronic deprivation of dust bathing leads to an uncontrollable condition of the lipids on the integument and an abnormal development of dustbathing. Such a deprivation therefore reduces animal welfare’. Furthermore, an association between dustbathing and feather pecking has been suggested (Vestergaard 1994). Rickets and osteomalacia resulting from calcium and Vitamin D deficiencies are problems in a number of captive species including basking reptiles. Direct exposure to natural light, and even indirect exposure to natural light remain the most effective means of promoting biosynthesis of Vitamin D for these animals (Bernard 1997).

Although theoretically the professed enrichment objective of allowing all animals to perform a full range of natural behaviours should result in a somewhat equal distribution of efforts to this end, this has clearly not been the case. Zoo environmental enrichment efforts and relevant research, as well as the formal evaluation of enclosure designs, have been heavily biased towards mammals, particularly primates (Sheperdson 1992; King 1993). The scanty research that has been done with zoo birds has largely focused on parrots (see section on bird enrichment studies).

Difficulties in objectively assessing the welfare state of an animal, or even the effect of enrichment efforts on its welfare state, are many (e.g. Dawkins 1990; Duncan & Poole 1990; Wiepkema & Koolhaas 1993; Barnard & Hurst 1996; Fraser et al. 1997; Robinson 1998). Not only are seemingly objective measurements of physiological and biochemical parameters often impractical to perform, their value as accurate indicators of the welfare state is highly questionable (e.g. Duncan & Poole 1990; Barnard & Hurst 1996).

Presence of abnormal behaviours is generally considered indicative of a poor welfare state (e.g. Duncan & Poole 1990; Broom 1991; Wiepkema & Koolhaas 1993), although this is arguably subjective (Barnard & Hurst 1996). Recognized abnormal behaviours in avian species include apathy, stereotypies, feather pecking, self-mutilation, mutilation or killing of conspecifics or other avian species and misdirected social preferences (King 1993; van Hoek 1995).

Experimental choice tests and operant conditioning are commonly used methods to evaluate environmental preferences of farm animals, and are in theory also applicable to zoo animals (Robinson 1998) as well as to caged birds. In practice operant conditioning experiments can only be carried out to a limited extent in zoos. The advantages and disadvantages of choice tests and operant conditioning experiments are discussed in a number of publications, for example Dawkins 1977; Duncan and Poole (1990); Barnard & Hurst (1996) and Robinson (1998). A method commonly employed by zoos to assess effect of environmental enrichment elements is comparison of time budgets of an animal during an ‘enriched’ period and a pre- or post- (or both) non-enriched control period. It is often possible to incorporate choice tests, for example of perching or food presentation preferences, into this type of study.

General data on location, locomotor activity and behaviours are commonly gathered to gain a more complete insight into any farther ranging spacio-temporal effects of an enrichment endeavour, rather than limiting observations to interactions directly related to the enrichment element. Time budget data from captive studies can be compared with time budgets of wild counterparts if these are available. This allows a global assessment of differences between captive and wild situations, but difficulties in collecting comprehensive, unbiased data for wild individuals arguably excludes use of these data as a reliable indicator of welfare (Veasey et al. 1996).

Inter-zoo comparisons between different zoo habitats for animals of the same species are a potentially fruitful and constitute an expanding field of research (Robinson 1998). Inter-zoo comparisons can be particularly useful in cases of neophobic taxa or in other situations for which the time-frame of the study does not allow for adequate assessment of the effects of changes in environmental conditions. For example a study of perching preferences of Crowned Pigeons Goura spp. carried out in four Dutch zoos indicated that individuals at one zoo with free choice of perching diameters almost invariably selected perches of diameters of 2 to 4 cm in diameter. A choice test was then performed to assess preferences of other crowned pigeons. This test was a failure because the pigeons were not observed to try any new perches for prolonged periods; in one zoo the observed latency period was seven weeks (Damen 1997).

Some studies to assess environmental requirements do not involve direct observation. For example, environmental features such as height, width and form of ledges designed to optimise reproduction, physical health and social interactions in a currently under-construction seabird enclosure at Rotterdam Zoo were derived from the literature, interviews and results of a seabird husbandry questionnaire answered by 15 zoos (King 1995). Gaining an understanding of an animal's ecology and determining its environmental requirements prior to designing its enclosure is crucial to incorporation of the animal's welfare needs into the design. If the design of an environment is appropriate to the animal's ecological requirements, relatively little ‘tinkering’ is later needed to provide the animal with opportunities to express a full range of behaviours (Robinson 1998). Some adjustments are in many cases necessary however, either because of unavailability of adequate information on the ecology to the animal or a lack of prior knowledge of how captivity would impinge on performance of a behaviour.

As above mentioned, elements that can be applied in enrichment of captive birds are physical structures integral to the enclosure design (e.g. shelters, plants, rocks and pools), impermanent objects (e.g. food items, balls, branches) and non-object stimuli (e.g. con- or heterospecifics, sounds, climatic and lighting variables). All of these categories can serve to evoke behaviours triggered by stimulation of one or more of the senses, and the combination can fulfil welfare considerations.

Poole (1992) put forth the following concerns for ensuring well-being (of mammals): stability and security, appropriate complexity, an element of unpredictability and opportunity to achieve goals. Physical structures largely provide stability and security and can address appropriate complexity and opportunity to achieve goals but elements of unpredictably and new opportunities to achieve goals are primarily provided through the more dynamic categories of enrichment elements. Other predictability, control, novelty and complexity properties desirable in enrichment elements (e.g. Wiepkema & Koolhaas 1993; Sambrook & Buchanan-Smith 1997) can also be met by supplying a combination of these environmental enrichment elements.

Suitability of specific elements to any given taxa is of course dependant on the ecology of that particular taxa. Some birds perform quite complex behaviours. Stamps et al. (1990) concluded from a study of early social relationships of fledgling budgerigars Melopsitticus undulatus that the sophisticated social behaviours of these birds are on par with that reported for mammals. Several species of parrots have proven able to solve ‘object permanence tasks’, indicating the ability to assimilate and use environmental information (Pepperburg & Kozak 1986; Pepperburg & Funk 1990). Psittacines are considered the ecological avian equivalent to primates (Birchall 1990; King 1992a). Their primate-like characteristics, which account for their popularity as companion birds, undoubtedly also explain the zoo environmental enrichment research emphasis on them. The Corvidae is another avian group renowned for its playfulness, intelligence and curiosity (Huxley 1945; Ficken 1977; Fagan 1981; Burton 1985) but nonetheless it has received little environmental research attention by zoos and members of this group are not often held as a cage birds.

Even if most birds are not considered intelligent by whatever definition of intelligence is used, ‘it does not follow that their minds are lacking in intensity or variety’ (Huxley 1947) or that they do not have a great number of interesting behaviours that could be elicited through environmental enrichment. Highly manipulative and diverse feeding behaviours prevalent in Ciconiiformes form one example. Use of bait and lures for catching prey by Green-backed Herons Butorides striatus has been documented on four continents and in the West Indies (Robinson 1994), capture of prey by use of bait has also been observed in the Saddlebill Stork Ephippiorhynchus senegalensis (D. Thompson pers. comm.) and probable tool use for prey capture by a Marabou Stork Leptoptilos crumeniferus has also been reported (Marshall 1982). Roseate spoonbills use as many as eight different feeding techniques (Hancock et al 1992).

Unfortunately the range of behaviours in the repertoire of an animal is often little known. There is no reference to play in Ciconiiformes in some reviews of avian play (Ficken 1977, Fagan 1981, Ortega & Bekoff 1987), yet all three forms of play described by Ortega & Bekoff- locomotor, object and social play-were observed in a study of behaviour of nestling and juvenile Ciconia spp. Furthermore an adult display, the ‘neck weave’ strongly resembling a form of juvenile and nestling play, and possibly constituting a form of adult solitary play, was also observed (King 1988).

Broad ecological characteristics can be drawn on to develop enrichment guidelines for a species when more detailed data are lacking and when the significance of the characteristics in relation to behaviour is understood. Robinson (1998) advocated approaching zoo animal enrichment from the generalist/opportunist vs. specialist view (as essentially proposed by Desmond Morris). Relative importance of a sense (sight, hearing, touch, taste and smell) in a given bird's general ecology can give some indication of suitability of enrichment items in the same way that they influence form of play (Fagan 1981) and other behaviours (Burton 1985). Ortega & Bekoff (1987) suggested that life history characteristics such as body size, degree of specialism, migratory habits, prevalence of nest helpers, and patterns of species-typical social organisation may influence elaboration of different types of play.

Mettke (1995) found that exploratory behaviour of psittacines was correlated with diet, habitat type and land form (mainland or island) but not with migratory behaviour or group size. Parrots feeding on cryptic or seasonal foods were more exploratory than those feeding on other foods, with species that feed on nuts (a cryptic food with variable handling time) being particularly exploratory. Species living in forest edge (a complex habitat) and islands were also found to be quite exploratory. Mettke made some recommendations for potentially suitable enrichment options in zoos based on her findings. Similar ecological behavioural patterns have been recognised less formally: Cravens (1993) classified parrots into three groups by their enthusiasm for chewing, and discussed this in relation to other behaviours and environmental considerations in holding them as cage birds.

In some cases use of general ecological traits or constraints to develop avian enrichment strategies might in fact be as useful as having some but incomplete information on a species. Rowley et al. (1989) found that, as might be expected, smaller cockatoo (Cacatuidae) taxa cope better with smaller seeds and larger taxa better with larger seeds in a study of seed preferences of eight Australian cockatoo taxa. However they also found that individual variation in preferences was high and overall results bore little relation to field observations of feeding behaviour. They suggested that the distribution, accessibility and abundance of different foods will often override preference rankings as will prior experience and example of others.

Static enrichment elements (physical structures) in an enclosure are often considered in the context of exhibit design, thus implementation is mainly accomplished within a limited time frame. A ‘program of requirements’ is now made for all new enclosures to be built at Rotterdam Zoo. The program is developed by a group consisting of the relevant biologist, department head, head keepers and botanical department. The purpose of these programs is to incorporate the ecological needs of the animals into the exhibit design, and to integrate them with other management requirements (e.g. for servicing of enclosures, capturing and handling the animals). An overview of the ‘program of requirements’ process relative to reptile exhibit design is provided by Visser (1998).

Certainly how playful or exploratory a bird is will influence its requirements for dynamic enrichment elements. These elements are the most difficult to provide over the long term (as their implementation is continuous) and therefore they receive the most attention, at least under the name of enrichment. The time and funds needed for acquisition or manufacture and replacement of impermanent objects and for provision of non-object stimuli often hamper their realisation.

An ‘enrichment group’ was thus developed in 1993 at Rotterdam Zoo to try to attack these problems and to stimulate environmental enrichment efforts. The complete group includes representatives from the keeping staff (working with a wide range of animal groups), the technical, botanical and biology departments, the animal department heads and the nutritionist. Meetings are held monthly; group members do not attend all meetings and some also only attend a portion of the meeting. The group is now experimenting with a ‘project’ approach to tackling issues.

In practice, most enrichment efforts that lead to an increase in locomotor, mandibular or vocal activity of birds are seen as positive, although stereotypies and most self-directed feather manipulations are not. Competence in social interactions and breeding behaviour are also often used as (usually informal) indications of how well the environment fulfils a bird's requirements.

Many dynamic avian enrichment efforts for zoo birds and presumably also cage birds focus on food. Foraging is a time consuming endeavour for many avian species; for example Glossy Cockatoos Calyptorhynchus lathami were found to spend 88% of the day engaged in feeding activities (Clout 1989). Therefore, prolongation the amount of time that a bird spends acquiring its food is in most cases a very suitable enrichment activity, particularly if employment of ecologically appropriate techniques to acquire the food are required. This approach can be quite simple but successful, i.e. hanging fruit for toucans or hornbills (Galama 1997) or provisioning different food in discreet patches throughout the enclosure for psittacines (Murray 1993). Live fish are very enthusiastically received by fish eating species, and even by some other carnivores that do not naturally incorporate much fish in their natural diets, e.g. Andean Condors Vultur gryphus (pers. obs.).

Hiding of food can also be an effective form of food enrichment, especially for species that feed on cryptic items. Inglis & Ferguson (1986) found that starlings Sturnus vulgaris preferred to search for food than eat freely available food; Coulten et al. (1997) recorded an increase in social behaviours (allopreening) associated with use of a variable and covered food supply in four species of parrots.

Enrichment novelty is easily achieved by provision of foods with different colours, textures, sizes and smells. However, many zoos (including Rotterdam Zoo) and private breeders are now moving towards feeding primarily pelleted diets to parrots (and other species). This is because of the nutritional problems that are still encountered when these birds can select items from a diet that is only balanced when all or most components are considered collectively (Schoenmaker & Hooimeijer 1998). Some zoos are now restricting non-pelleted or non-balanced dietary items to 5-20 % of the energy (in kcal) of the available diet (e.g. Sheppard 1994; Nijboer 1998). This means that the proportion of the diet that provides variation as a form of enrichment is quite restricted, and most be used wisely.

Areas that have been little explored but seem to have great welfare implications and potential enrichment possibilities for captive birds are climatic variables and different aspects of lighting, as investigated in a reproductive study of Cockatiels Nymphicus hollandicus (Millam et al. 1988), and a study of lighting preferences of poultry (Manser 1996). Other ecological requirements that are very basic to a bird's welfare are often either not well understood or not adequately addressed in provision of enrichment elements and still deserve attention. For example provision of suitable perching for farm poultry remains problematic and a number of studies in this area have recently been carried out, as summarised in Lambe & Scott (1998). Some student projects addressing perching concerns for various birds have been carried out at Rotterdam Zoo in this decade.

Sounds constitute a relatively unexplored source of avian enrichment possibilities. Sequeira (1994) found that the sound of a running waterfall elicited flying activity of young Masked Lovebirds Agapornis personata. Play back vocalisations of the infrequently emitted ‘cry’ vocalisation of Congo Peafowl Afropavo congensis have been highly effective in stimulating locomotor activity and vocalisations of this species (Kuiper 1997; pers. obs).

A number of studies that have had positive influences on bird behaviour have involved changes in more than a one variable at the same time, thus although the benefits of enriching the environment are demonstrated the relative importance of the different forms of environmental enrichment used are not: e.g. decrease in autopreening frequency, increased performance of object-oriented behaviours and visibility of a female Blue-eyed Cockatoo Cacatua opthalmica (King 1992b); increased activity and willingness to approach unfamiliar conspecific budgerigars (Nicol & Pope 1993); improved reproductive performance in first time breeding Orange-winged Amazons Amazona amazonica (Millam et al. 1995). Diet and presence of nest boxes in otherwise non-stimulatory conditions were ruled out as factors that affected breeding activity in a series of experiments performed with cockatiels, however any one or a combination of four other environmental factors could have been responsible for the observed higher breeding success of the environmentally manipulated study group (Millam et al. 1988).

There have been a few studies in which the changes in behaviour are more easily correlated with a single environmental variable. Locomotor activity, vocalisation and singing was found to be higher in Zebra Finches Poephilia guttata housed in cages with relatively complex cage furnishings, and more flying was also seen in a large enriched cage (Jacobs et al. 1995) however only one pair of birds was studied per treatment. In a study of the effect of two different forms of enrichment (foods and toys vs. perches) on behaviour of Crimson-bellied Conures Pyrrhura perlata perlata it was found that enrichment in the form of foods and toys resulted in a desired decrease in preening and presence of natural perches in a desirable increase in locomotion. The best results (increased locomotion and decreased autopreening) were achieved with a combination of the two enrichment methods (van Hoek & King 1997).

Social relationships between, and individuality of, animals undoubtedly influences responses to enrichment items. Inter-individual differences in responses to enrichment items have been found to be quite common in captive studies in which sample sizes are relatively small (e.g. Murray 1993; Rowley et al. 1989; Sequeira 1994; Coulten et al. 1997). Mettke (1995) did not detect inter-individual differences in her study of exploratory behaviour of psittacines, but because social dominance was quite important in determining exploratory behaviour only the most dominant bird per cage was included in her analysis. As she noted, multiple enrichment items often need to be provided in enclosures to allow all group members access to enrichment items.

An increase in exploration of novel objects with some habituation to the objects has been observed for various psittacine species (Sequeira 1994; Mettke 1995). Van Hoek & King (1997) found that natural enrichment items (e.g. foods and branches) were preferred over non-natural toys by Crimson-bellied Conures, however it is difficult to determine whether or not the preference was determined by experience, as the birds had previous exposure to only the natural items. Studies of species characteristic responses to novel space and structures such as that reported for ravens Corvus corax by Szedlarik & Kortschal (1997) could be useful in anticipating responses to enrichment elements introduced in enclosures.

There is much to be learned regarding environmental enrichment and attention to welfare considerations in birds. Some very basic ecological requirements (e.g. suitable perching) still deserve attention. Other areas that would seem particularly useful to investigate include development of enrichment guidelines based on general ecological characteristics of a species, and studies to more precisely define the influence of enrichment elements on specific behaviours of the birds receiving them.

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