Guidelines and Ethical Considerations for Housing

Guidelines and Ethical Considerations for Housing and Management of Psittacine Birds Used in Research Isabelle D. Kalmar, Geert P.J. Janssens, and Christel P.H. Moons

Abstract The Psittaciformes are a large order of landbirds comprising over 350 species in about 83 genera. In 2009, 141 published studies implicated parrots as research subjects; in 31 of these studies, 483 individuals from 45 different species could be considered laboratory animals. Amazons and budgerigars were by far the most represented psittacine species. The laboratory research topics were categorized as either veterinary medicine and diagnostics (bacteriology, hematology, morphology, and reproduction; 45%) or behavioral and sensory studies (behavior, acoustics, and vision; 17%). Confinement of psittacine species for research purposes is a matter of concern as scientifically based species-specific housing guidelines are scarce. The aim of this article is to provide scientific information relevant to the laboratory confinement of Psittaciformes to promote the refinement of acquisition, housing, and maintenance practices of these birds as laboratory animals. We briefly discuss systematics, geographical distribution, legislation, and conservation status as background information on laboratory parrot confinement. The following section presents welfare concerns related to captive containment (including domestication status) and psittacine cognition. We then discuss considerations in the acquisition of laboratory parrots and review important management issues such as nutrition, zoonoses, housing, and environmental enrichment. The final section reviews indications of distress and compromised welfare. Key Words: avian welfare; bird; enrichment; housing; laboratory animal; nutrition; parrot; psittacine

Introduction

T

he Psittaciformes or parrots form a large order of land birds comprising over 350 species in about 83 genera (Collar 1997). In the United States they are the third

Isabelle D. Kalmar, Msc Vet Med, MSc LAS, is an assistant in the Laboratory of Animal Nutrition; Christel P.H. Moons, PhD Vet Med, MSc AS Lic, is an assistant professor in the Laboratory of Ethology; and Geert P.J. Janssens, PhD Vet Med, agr eng, is a professor in the Laboratory of Animal Nutrition, all at Ghent University in Belgium. Address correspondence and reprint requests to Isabelle Dominique Kalmar, Laboratory of Animal Nutrition, Department of Nutrition, Genetics, and Ethology, Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium or email [email protected].

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most popular companion animal, estimated at 10.1 million individuals in 2002 (AVMA 2002). Although their confinement in laboratory settings for research purposes is believed to be limited, it is a matter of concern because scientifically based species-specific housing guidelines are scarce. According to the Universities Federation for Animal Welfare Handbook on the Care and Management of Laboratory and Other Research Animals (UFAW 2010), a laboratory animal in the broadest sense is “any non-human member of the animal kingdom which is kept in captivity for experimental or observational purposes.” Accurate information on the extent of psittacine bird use in laboratory research is lacking because official statistics on laboratory animals do not specify psittacine birds. For this review we performed an ISI Web of Knowledge literature search in January 2010, using the search string “Topic=(psittaci*) OR Topic=(parrot*)” and including all 2009 references. This search yielded 141 database entries, which we categorized into type of research and research field as shown in Table 1. The main research fields in laboratory experiments were veterinary medicine and diagnostics (bacteriology, hematology, morphology, and reproduction; 45%) and behavior and sensory studies (behavior, acoustics, and vision; 17%). As shown in Figure 1, studies published in 2009 in which parrots were used as laboratory animals involved 483 individuals of 45 different psittaciform species. Because it was not possible to determine the number of animals used in three studies, the total number shown is a slight underrepresentation of the actual count of laboratory Psittaciformes. Most animals (83%) belonged to the Psittacidae family, and 12% and 5% of individuals belonged to the families Cacatuidae and Nestoridae, respectively. Within the Psittacidae, most of the subjects (97%) were true parrots (only 12 individuals were lorikeets), and of these Amazons (38%) and budgerigars (32%) were by far the most represented. We also summarized information on the type of housing described in the 31 publications of 2009 that cited the use of parrots in laboratory experiments (i.e., not field studies or other types of research). We found that 42% (n = 13) of the parrots were housed at on-site facilities, 23% (n = 7) at offsite facilities, and for 35% of cases (n = 11) housing information was unavailable. The off-site facilities were all outdoor aviaries; most studies conducted at on-site facilities used indoor cages (59% or n = 4), only 23% (n = 2) used outdoor confinement, and in 18% of the studies (n = 1) this information was unavailable. Information on group housing 409

Table 1 Number of peer-reviewed studies published during 2009 involving Psittaciformes as subjects sorted by research type (rows) and research field (columns) VMD Field study

BS

EC

GEN

NUTR

Total (%)

4

6

32

4

1

47 (33%)

Laboratory experiment

11

16

0

2

2

31 (22%)

Opportunistic sampling

17

1

0

10

0

28 (20%)

Case report

23

1

0

0

0

24 (17%)

8

0

1

2

0

11 (8%)

63

24

33

18

3

141 (100%)

Undetermined Total

BS, behavior and sensory; EC, ecology; GEN, genetics; NUTR, nutrition; VMD, veterinary medicine and diagnostics

was provided in 61% (n = 19) of the studies: 19% (n = 6) used individual housing, 13% (n = 4) pair housing, and 29% (n = 9) group housing. The aim of this article is to provide scientific information concerning laboratory confinement of Psittaciformes, with the intention of refining arrangements for their acquisition, housing, and maintenance. We begin with an overview of systematics, geographic distribution, and specific legislation and conservation status. The next section presents a discussion of welfare concerns related to captive containment, including psittacines’ domestication status and cognition. We then discuss factors to consider in the acquisition of laboratory parrots, followed by a review of important management issues related to nutrition, housing, and environmental enrichment. The final section concerns zoonotic diseases and indications of distress and compromised welfare.

Background Information Systematics Psittaciform birds have distinct morphological traits, such as a stout curved beak topped by a cere (the bump where the nostrils are located), zygodactyl feet (two toes pointing forward and two backward), and colorful plumage. Traditionally, psittacines are phylogenetically placed between the Columbiformes (pigeons) and Cuculiformes (cuckoos). Using molecular techniques, Sibley and Ahlquist (1990) suggested a closer relationship with Apodiformes (swifts), but this would be inconsistent with the plesiomorphic or primitive distal centriole in swift sperm (Jamieson and Tripepi 2005). Within the order of Psittaciformes, two distinct groups are generally recognized as separate families: Cacatuidae (cockatoos) and Psittacidae (Collar 1997; Forshaw and Cooper

Figure 1 Total number of Psittaciform individuals (n) and species (N) included as study subjects in peer-reviewed studies published during 2009. For one study using Amazon parrots and for two from the “other” category the exact sample size could not be derived; the resulting underrepresentation of the actual count is shown in italic font. 410

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2002). External morphological features of cockatoos that distinguish them from other parrots include an erectile crest and lack of Dyck texture1 in feathers (as a result of the latter, cockatoos never display blue or green colors in their plumage). Internal differences include the presence in cockatoos of a gallbladder, which is absent in other parrots (Rowley 1997). Recent phylogenetic data (Tokita et al. 2007) suggest a third family in the order of Psittaciformes, the Nestoridae, which includes the New Zealand parrots: kakapo (Strigops habroptilus), kea (Nestor notabilis), and kaka (N. meridionalis). Lories and lorikeets are a separate group, distinguished by certain anatomical features and feeding preferences, but their classification into a subfamily within the Psittacidae (loriinae) or into a separate family (Loriidae) is controversial (Russell 1987; Forshaw and Cooper 2002). The most prominent anatomical characteristic of lories is their long, brush-tipped tongue and slender beak, reflecting a high degree of diet specialization toward nectar and pollen (Cornejo and Clubb 2005).

Geographic Distribution Most Psittacines are native to the southern hemisphere and are predominantly, but not exclusively, found in tropical regions. Lories, lorikeets, and cockatoos occur naturally only in Australia and surrounding Indonesian islands. Genera in the family of Psittacidae, on the other hand, are indigenous to Asia, Central and South America, Africa, and the Australian continent. There are only two genera of Asiatic parrots: hanging parrots (Loriculus spp.) and ring-necked parakeets (Psittacula spp.). Pionus parrots (Pionus spp.), macaws (e.g., Ara, Cyanopsitta, and Anodorhynchus spp.) and conures (e.g., Aratinga, Cyanoliseus, and Pyrrhura spp.) are native to South America, and the Amazons (Amazona spp.) originate from Central and South America. African greys (Psittacus spp.), Poicephalus parrots (Poicephalus spp.), and lovebirds (Agapornis spp.) originate from Africa; grass parakeets (Neophema spp.), budgerigars (Melopsittacus sp.), and rosellas (Platycercus spp.) are indigenous to Australia (Russell 1987). Irrespective of geographical origin, descendants of escaped cage birds have been establishing self-sustaining populations in regions other than their native habitat. For instance, monk parakeets (Myopsitta monachus), which are indigenous to South America, have formed feral populations on four other continents (Russello et al. 2008), and in the United States the American Ornithologists’ Union (www.aou.org) has identified seven parrot species as selfsustaining exotic species, with another seven likely to be recognized as such in the near future. But the two native US parrot species, the Carolina parakeet (Conuropsis carolensis) and the thick-billed parrot (Rhynchopsitta pachyrhyncha), disappeared during the 20th century (Butler 2005). Although efforts to reestablish the latter have not resulted in self-sustaining wild populations, release experiments with

wild-caught birds from Mexico, where the species is still extant, have resulted in a limited number of surviving, translocated birds and some reproductive success in Arizona (Snyder et al. 1994).

Conservation and Legislation Parrots have become the most endangered birds in the world—almost all species in the order of Psittaciformes are listed by the Convention on International Trade in Endangered Species (CITES2), an international treaty that classifies endangered species and regulates the import and export of wild flora and fauna, including animals (alive or dead) and their products and tissues. CITES Appendix I (also called CITES I) lists species at risk of global extinction; Appendix II includes (1) species that may become threatened with extinction in the absence of international trade restrictions, (2) nonendangered species that may be in danger because of their resemblance to specimens listed in the appendices, and (3) second-generation captive-born offspring of Appendix I species (CITES 1973, 2009); and Appendix III lists species for which trade is regulated in specific countries. Appendix I lists 51 psittacine species, which account for about one-third of all avian species in this CITES appendix; nearly the entire remaining two-thirds of psittacine species appear in Appendix II (CITES 2009). Only four species of Psittaciformes are not considered at risk: peach-faced lovebirds (Agapornis roseicollis), budgerigars (Melopsittacus undulatus), cockatiels (Nymphicus hollandicus), and rose-ringed parakeets (Psittacula krameri). The acquisition, transport, housing, and care of animals kept for research purposes (and the reporting thereof) are subject to national legislation. In the United States, any vertebrate animal use in research, teaching, or testing is considered experimental and therefore subject to legal requirements. But coverage of birds in the US Animal Welfare Act (AWA), which regulates the treatment of laboratory animals in the United States, has been a subject of debate as the Act’s original definition of “animal” did not include birds. Subsequent amendments only partly addressed this exclusion: the Act now covers birds not bred for research purposes, but explicitly excludes birds bred for research (Cohen 2006). US research facilities that receive federal funding also have to comply with the Public Health Service policy, outlined in the Guide for the Care and Use of Laboratory Animals (NRC 1996). The stipulations of the latter, in contrast to the AWA, also include purpose-bred birds (Federal Register 2004) but lack species-specific guidelines on housing and management.3 In contrast to US guidelines and restrictions, European legislation excludes noninvasive procedures as well as humane euthanasia, classifying only procedures that inflict 2Abbreviation

used in this article: CITES, Convention on International Trade of Endangered Species 1Blue

feather color is formed by nanostructures in the feather called Dyck texture (Dyck 1971a,b).

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3The recent update of the Guide (8th ed., NRC 2010) includes references for readers interested in this information for birds.

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pain, suffering, distress, or lasting harm as animal experiments (European Community 1986). Additional legislation governs the import and export of endangered Psittaciform species as well as their scientific use. The US Fish and Wildlife Service, through a permit system, governs the import, export, and interstate trade of species listed as endangered or threatened in the United States or elsewhere under the Endangered Species Act and is also responsible for CITES administration (NRC 2006). Import or export of Appendix I specimens is allowed under very strict permitting requirements only for scientific purposes, education, or conservation, but not commercial trade (ARENA/OLAW 2002; NRC 2006). In Europe, CITES I specimens may be used in animal research only if (1) the objective is to preserve the species or (2) the species is the only available model in fundamental biological studies (European Community 1986). A number of regulations govern the use of birds, both wild caught and captive bred. In Europe, the scientific use of CITES-listed wild-caught birds or their eggs is permissible only if they are essential to the research and all necessary licenses have been granted by the appropriate authorities (European Community 1979). In the United States, importation of CITES-listed avians (with some exceptions, including 37 captive-bred parrot species) requires a Wild Bird Conservation Act permit. The Lacey Act, on the other hand, which concerns injurious birds (those that cause damage to indigenous flora and fauna), does not apply to either birds imported for scientific research or psittacines imported for any purpose. Irrespective of purpose, US importation of birds requires a 30-day quarantine period (except for imports from Canada); importantly, if a single bird in the lot is diagnosed with highly pathogenic avian influenza or Newcastle disease during the quarantine period, the whole lot must be destroyed (Paul 2005). Further information about legislation is available (NRC 2006; Paul 2005).

Main Areas of Welfare Concern Domestication Parrots, commonly admired for their vocal abilities and exotic appearance, have been kept in captivity for at least 2500 years. The first parrots introduced into Europe were probably Alexander parakeets (Psittacula krameri), brought from the Far East by Alexander the Great during the 4th century BCE; North African and Indian species were spread by the Romans. In the 15th and 16th centuries, European explorers brought back American and Asian parrot species as living proof of their voyages (Collar 1997; Forshaw and Cooper 1989; Silva 1991), and in the 18th century colonists brought small Australian parakeets to Europe by (Silva 1991). Budgerigars were successfully bred in captivity by the end of the 19th century, largely because of their early reproductive maturity and sexual dimorphism (Alderton 2001; Earle and Clarke 1991; Silva 1991). Captive breeding in 412

other parrot species, however, has become truly successful only in the past 40 years. Aside from their late maturity and sexual monomorphism to the human eye, other contributing factors to this delay are the animals’ strict monogamy and need for prolonged periods of parental care. A major improvement in captive breeding was the development of endoscopic and genetic sexing, as well as histological appraisal of breeding potential from testis biopsies. Thanks to these developments, about 85% of parrot species have bred in captivity (Crosta et al. 2002; Gartrell 2002; Harcourt-Brown 2000; Silva 1991). Yet domestication—the process of adaptation to captivity through genetic changes—is still in its infancy for parrots and other psittacines (Meehan et al. 2003b). Although parrots have been bred for generations and can become very docile and adapted to captive environments within their lifespan, they still share natural behavior and response thresholds with their wild counterparts and should be considered wild animals (with the possible exceptions of budgerigars and cockatiels; Bergman and Reinisch 2006). In contrast to dogs and cats, for example, parrots are still in their first few captive-bred generations and have not yet undergone selection for behavioral traits that facilitate adaptation to life in captivity (Davis 1999). They are therefore likely to experience frustration when confined in conditions that limit the expression of species-specific behaviors, especially those associated with high levels of motivation.

Cognition The remarkable cognitive abilities in psittacine birds, which have been intensively studied and documented (e.g., Giret et al. 2009; Pepperberg 2009; Shuck-Paim and Borsari 2009), can be a source of welfare concern in the laboratory and necessitate careful consideration of the choice of species and housing conditions. Parrots’ vocalizations, and especially their ability to mimic the human voice, are a distinctive manifestation of their cognition,4 and they exhibit lifelong vocal learning, whereas in most songbirds this feature is limited to a sensitive period in early development (Marler 1970; Scarl and Bradbury 2009). In the oldest known writings about parrots, dating from 500 BCE, Ctesius described a plum-headed parakeet (Psittacula cyanocephala) saying Indian and Greek words (Collar 1977). Scarl and Bradbury (2009) suggest that the ability in some parrot species to mimic vocal calls in a single interaction is an efficient vocal technique for mediating fissionfusion flocks (constantly changing social groups). And Schachner and colleagues (2009) demonstrated the ability to align synchronized motor actions (head movements and foot lifting) in response to music in an African grey parrot (Psittacus

4This ability in psittacines is distinctive but not unique: songbirds (Passeriformes)

and hummingbirds (Trochilidae) also display vocalization through imitation (Matsunaga and Okanoya 2009), in contrast to the vocalizations of most avian groups, which depend on the production of innate sounds.

ILAR Journal

erithacus erithacus) and a sulfur-crested cockatoo (Cacatua galerita). In addition, numerous scientifically sound laboratory studies of parrot cognition have demonstrated that several parrot species display a much higher intellectual capacity than the ability merely to mimic the human voice. The African grey parrot Alex is probably the best-known individual in this research. Pepperberg (2006) worked extensively with Alex and reviewed his trained cognitive abilities, which included the labeling of over 50 objects and the functional use of short queries that demonstrated accurate comprehension of concepts such as color, shape, material, relative size, and quantity. Studies of other African greys have demonstrated mirror-mediated discrimination, spatial location, and spontaneous categorization into unlabeled edible or nonedible items (Giret et al. 2009; Pepperberg 1995). Although most cognitive research in parrots has involved African grey parrots, advanced cognitive processing has been evaluated on other parrot species as well. Werdenich and Huber (2006), for instance, showed successful performance of complex string-pulling tasks in keas, and Shuck-Paim and Borsari (2009) demonstrated this ability in neotropical parrot species (two macaw and one Amazon species). The cognition of parrots is consistent with several characteristics generally associated with advanced cognitive processing, such as a relatively large brain, slow development, longevity, and a long period of parental association (ShuckPaim and Borsari 2009).

Factors to Consider in the Selection of Laboratory Parrots The acquisition of animals that will be confined in laboratory facilities for research purposes should always be based on careful consideration of the species, source, and proposed use and should take into account species, age, gender, background, and homogeneity of these features among the birds to be used. Purchases should not depend simply on ease of availability or proximity of a retailer. Most importantly, whenever possible, the least endangered and least cognitively developed species should be the species of choice consistent with achieving the experimental goals. In addition, several other factors are important to consider. First, a heterogeneous group of laboratory animals is likely to increase variability of research or test results and thus decrease the strength of experimental setups (and possibly require the use of additional animals). Second, good knowledge of the animals’ background improves interpretation of research data and promotes sound decisions on necessary health measures, which may considerably reduce the likelihood of introducing infectious agents into the resident colony. Third, poor socialization may influence the animals’ aptitude to undergo laboratory confinement or may hamper the ease of handling. In our opinion, appropriate socialization of birds is of utmost importance in their laboratory confinement. Socialization facilitates handling by animal Volume 51, Number 4

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caretakers, enhances the performance of experimental procedures, and reduces the risk of development or aggravation of welfare issues. In addition to all of the above factors, it is advisable to consider the following species traits when acquiring laboratory parrots: species size, ecology, behavior, anticipated longevity, and suitability for the intended research. Bird size, ecology, and behavior can affect the ethics of a decision about the housing of certain species in the available space; solitary housing, which is necessary in some research, can be deleterious to the well-being of certain species. Further, the loudness of normal vocalization varies by species (African grey parrots, for instance, are quieter than most Amazons and cockatoos) and may require thoughtful consideration if the animal housing area is near research offices (Wilson 2006). It is especially critical to bear in mind that all parrots are long-lived animals (Carpenter et al. 2001), and some species more so than others; budgerigars, for instance, have a relatively short lifespan (8 to 10 years) in contrast to the larger parrots (50 to 80 years). Longevity may thus be an ethical consideration when choosing a parrot species, as most are very likely to outlive the duration of a research project. We recently reviewed possible fates of laboratory parrots after the completion of research projects and found the following options: relocation to private care or zoological collections, humane euthanasia, or reintroduction to the natural habitat (Kalmar et al. 2007a). The first option is considered the most ethical choice, but may not be feasible if responsible research personnel did not socialize the birds properly during their laboratory confinement (Kalmar et al. 2007a). Finally, the selection of appropriate parrot species for laboratory use can depend on their susceptibility to a particular infectious or metabolic disease. For example, African grey parrots may develop hypocalcemic tetany syndrome in response to an absolute or relative calcium deficiency; other parrot species respond to such a deficiency with calcium mobilization from their bones, thus maintaining blood calcium level but developing metabolic bone disease (Kollias 1995; Levine 2003). The peculiar calcium metabolism in African greys makes this species an outstanding model to investigate its underlying mechanisms. In conclusion, the selection of appropriate birds for laboratory research should take into consideration not only the most suitable species but also the individual’s features for the intended research to optimize both the experimental data and animal welfare.

Management Considerations Nutrition Obesity and nutritional deficiencies are a common cause of disease in captive parrots. Without a well-considered feeding strategy, nutritional imbalances will occur and adversely affect animal health and welfare as well as experimental results. 413

Parrots are commonly fed a multicomponent whole-seed diet, which is perceived as a natural diet because parrots are classified as seed eaters. But commercial parrot food mixes of cultivated seeds and nuts differ significantly from the natural diet of wild parrots, which consume a wide range of plant parts as well as invertebrates and sometimes meat from animal carcasses. Their diet also changes based on seasonal availability (Collar 1997; Ullrey et al. 1991). Moreover, the typical ingredients in commercial seed mixes for parrots are often not indigenous to the natural habitat of all parrot species for which these mixes are intended. Sunflower seed, pumpkinseed, and peanuts, for instance, originate from the American continent and thus are not natural food items for African, Australian, or Asiatic species. Additionally, physical constraints would hamper wild parrots’ foraging on peanuts or pumpkinseeds, which captive parrots regard as preferred food items (Kalmar et al. 2010). Regardless of the type of diet, fresh food should be provided daily, and clean drinking water must be available at all times and refreshed at least daily. Effect of Nutrition on Feather Color In contrast to several other bird orders, where red, yellow, and orange feather pigment is a function of dietary-derived carotenoids or metabolites thereof (McGraw et al. 2004), the feather coloration of psittacine birds cannot be influenced by dietary supplements (although aberrant pigmentation often reflects chronic malnutrition or toxicity; for review, Koski 2002). Over 80% of psittaciform species display red in their feathers; in parrots this color is generated by unique red pigments, called polyenal lipochromes or psittacofulvins, that are locally synthesized de novo at maturing feather follicles (Forshaw and Cooper 1978; Stradi et al. 2001). Blues, on the other hand, are formed by feather nanostructures (Dyck texture) and greens evolve from a mixture of the blue structural color and endogenously produced yellow pigments (Dyck 1971a,b; McGraw and Nogare 2005; Rowley 1997). Black, brown, and grey shades result from melanin pigmentation, whereas unpigmented feather keratin is white (McGraw et al. 2005; Prum et al. 1999). Psittacine Strategies in Detoxification of Foodstuffs Parrots’ inherent tendency to peel food items is thought to be a method to safely broaden their repertoire of forageable food items (to include, for example, seeds that are toxic to other species) as the outer layers of certain plant products often contain the highest concentration of toxins (Gilardi et al. 1999). Other natural methods of detoxification include ingestion of clay or charcoal, which adsorb potential dietary toxins and may confer cytoprotection of the gastrointestinal lining (Collar 1997; Gilardi et al. 1999). Burger (2003) and Mee and colleagues (2005) further substantiate intake of clay in parrots as a deliberate defense mechanism against secondary toxic 414

plant compounds, because geophagy typically occurs before foraging. Brightsmith and Muñoz-Najar (2004) posit the provision of additional sodium and other minerals when the dietary supply is insufficient as a further function of geophagy, suggesting a degree of innate nutritional wisdom.

Seed Diets Commercial seed mixtures commonly provided to, and readily ingested by, parrots are deficient in several minerals and vitamins, and contain a deteriorated calcium:phosphorus ratio (e.g., Harrison 1998; Ullrey et al. 1991; Wolf et al. 1998). Manifestation of resulting deficiencies remains subclinical for prolonged periods of time, and when clinical symptoms do emerge they are often unspecific and remain undiagnosed (Wolf et al. 1998). It is thus not surprising that malnutrition constitutes the primary cause of up to 90% of all clinical problems in pet birds presented to veterinarians (Harrison 1998). In addition, because parrots dehusk seeds (thereby consuming only the kernel) and display a profoundly selective feeding behavior when provided a multicomponent diet, preferring oilseeds (e.g., pumpkin and sunflower seeds) over carbohydrate-rich seeds, the fraction they actually consume is significantly different from the intended diet. They also consume inadequate amounts of supplements (e.g., oyster shells or vitamin-, amino acid-, and mineral-rich pellets) incorporated in these seed-based diets (Kalmar et al. 2010). Nutritional supplementation through drinking water is not recommended as vitamins are unstable in aqueous solutions and reduce water palatability, possibly decreasing water intake and introducing a risk of dehydration (Donoghue and Stahl 1997; Hawley 1997).

Pellet Diets: Advantages Pellet diets rather than seed mixtures are strongly recommended for birds used in laboratory research because they offer two important advantages: they prevent selective feeding behavior and they can be precisely formulated to comply with available nutrient guidelines (e.g., AAFCO 1998). As a result, first, the pellet diet can contribute to long-term health and help reduce biased research data that may result from (undiagnosed) dietary deficiencies. Second, with a multicomponent diet, management and/or animal factors may result in a significant divergence between the nutrient supply (known) of the offered diet and that of the actual consumed fraction (unknown unless specifically calculated based on analysis of food intake, nutrient content of offered diet, and a subsample from the total collection of all food remainders). Such analyses are costly, time intensive, and inevitably inaccurate when birds are group housed. Seeds, nuts, fruit, and some vegetables can be provided as treats to complement the pellet diet; fruit can be offered ad libitum as a safe measure to reduce voluntary energy intake and prevent obesity without compromising sufficient protein intake (Kalmar et al. ILAR Journal

2010). However, avocado,5 for instance, is highly toxic to parrots (Hargis 1989; Schulte and Rupley 2004). Pellet Diets: Responses to Concerns Despite the advantages of pelleted food in terms of nutrition as well as easy dosing and delivery of oral test substances, several concerns about such diets persist. We address these based on published reports and our own observations. First, there is concern that the lack of a husk on pellets might compromise parrots’ natural feeding behavior, which includes manipulation of food with their feet and beak. But parrots intensively manipulate pellets before ingestion, which is consistent with their behavior when they eat seeds or nuts (Rozek et al. 2010). Second, a potential reduction in the animals’ time spent feeding might result in boredom and behavioral disorders. However, Wolf and colleagues (2002) demonstrated similar feeding time budgets when parrots were fed either seeds or pellets; and increasing the size of the pellets can contribute to a rise in total time spent feeding (Rozek et al. 2010). Third, parrots are notably neophobic, especially when wild caught, single housed, or raised in barren environments (Fox and Millam 2004; Meehan and Mench 2002; Meehan et al. 2003a), so it is in their nature to be resistant to novel food items (i.e., a change from a seed diet to a pellet diet). But most parrots can be readily and safely converted to pellet diets with a proper conversion schedule and careful monitoring of their food intake. Conversion of food type is not recommended for birds housed in large groups in which individual monitoring is impeded and must be avoided with sick birds (Ghysels 1997). Last, the fact that pellet feeding has been shown to inflict gastric lesions in other granivorous birds (i.e., chickens; Bird et al. 1937) raised concerns that the same might be true for parrots. However, parrots use their beaks to reduce the particle size of ingested foodstuffs, whereas chickens ingest grains whole and reduction of ingredient size normally occurs in the gizzard (through its strong musculature and thick koilin layer, assisted by the mechanical action of ingested grit). Hence, it is likely that particle size reduction through food processing during the manufacture of pellets (which are simply compressed or extruded forms of ground ingredients) has far less effect on the gizzard in parrots compared to chickens (Kalmar et al. 2007b). Diet Specialization in Minor Parrot Groups Some groups of parrots have particular feeding specializations. Among the Nestoridae, the nocturnal and flightless kakapo is entirely herbivorous and feeds mostly on tree leaves, grasses, and herbs, ingesting only the plant juices and spitting out squeezed pellets containing coarse fibers (Eason et al. 2006; Houston et al. 2007). In contrast, the kea is 5The

avocado pit contains the toxin persin, which leaks into the fruit and is cardiotoxic to birds (Schulte and Rupley 2004).

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omnivorous and the kaka forages on diverse plant items as well as large numbers of invertebrates (Diamond and Bond 1991; Moorhouse 1997). The Loriidae or loriinae are nectarivorous birds (i.e., they feed predominantly on nectar and pollen), supplementing their intake with fruit, flowers, and invertebrates as minor components of their diet (Cannon 1984; Collar 1997; Gartrell 2000). In captivity, lorikeets are usually fed a commercially available nectar powder that is diluted before use; the degree of dilution affects voluntary intake and thus energy and nutrient supply (Kalmar et al. 2009). Food Storage The method of storage can vastly alter the nutritional composition of the manufacturer’s formulation because food is often stored in large containers in which different-sized ingredients segregate. It is therefore advisable to regularly stir the food and completely empty storage containers of multicomponent diets before refilling to ensure that all components are eventually fed to the animals. An alternative option is to store food in the original bags (Kalmar et al. 2010), although closed feed containers offer the advantage of improved protection against vermin. Food should be properly stored and consumed (or disposed of) by the manufacturer’s indicated date, as improper (i.e., suboptimal temperature or relative humidity) or prolonged storage can promote the formation of mycotoxins (Samour 2004). Exposure to air or light also negatively affects the nutritional quality of foods, for example by reducing the content of several vitamins (Reddy and Love 1999). According to Bavelaar and Beynen (2003), oxidation of polyunsaturated fatty acids due to improper storage is likely to be more extensive in pelleted foods compared to seeds as the husks of the latter protect fatty acids from exposure to air.

Zoonoses Like many laboratory animals psittacine birds can be carriers of infectious agents with zoonotic potential (i.e., transmissible to humans). A complete overview of such zoonotic agents falls outside the scope of this article; instead we offer general guidelines, with a brief description of psittacosis (also called ornithosis), which is possibly the most significant zoonosis associated with parrots (Scott 1995; Turner 1987). All personnel should be well informed of the possible risk of zoonotic diseases, which can be contracted either directly from psittacine birds or indirectly from their excreta or contaminated materials and air. Adequate personal and environmental hygiene measures—including vermin control, as the latter also can be vectors of disease—should be in place at animal facilities. Personnel with impaired immunity, including pregnant women, should strictly avoid any direct or indirect contact with the birds. Newly acquired parrots should be subject to appropriate quarantine and screening procedures. Such measures enable 415

Housing

early identification of possibly zoonotic agents and may prevent the transmission to resident birds of infectious agents (e.g., psittacine circovirus, which causes beak and feather disease). To protect the health of both personnel and birds, animal health checks, including diagnostic screening for important zoonotic agents, should be repeated regularly. Table 2 provides a partial list of zoonotic agents that can be contracted from parrots (Scott 1995). Of particular importance is Chlamydophila psittaci, which is the etiologic agent of the human disease psittacosis (also called parrot fever and ornithosis). Parrots can be asymptomatic carriers and shedders of chlamydiosis, and the strains found in Amazon parrots seem to be particularly virulent to humans (Turner 1987). In birds the disease is usually a subclinical infection but may be associated with nonspecific clinical signs such as dyspnea, anorexia, lethargy, diarrhea, biliverdinuria (yellow to green urates), and oculonasal discharge (Gould 1995; Greenacre 2003; Turner 1987). In humans the infection usually also passes subclinically, but clinical signs may vary from mild respiratory disease to pneumonia, nausea, vomiting, hepatitis, myocarditis, disorientation, mental depression, delirium, and even death. Possible transmission routes of C. psittaci from birds to humans include, in order of importance, inhalation of contaminated air; direct contact with birds, feathers, excreta, oculonasal discharge, or infected tissue; and bites or other open wounds. The incubation period is 1 to 4 weeks (Turner 1987). Diagnostic tests for C. psittaci in parrots include culture, cytology, polymerase chain reaction, and the enzyme-linked immunosorbent assay, but none of these has proven to be 100% accurate (Gould 1995; Turner 1987).

Despite their widespread geographic distribution, most parrot species have similar behavior repertoires and thus similar housing and management requirements in captivity (Russello et al. 2008). Parrots are generally diurnal prey animals and, with few exceptions, highly social birds that establish strong, monogamous pair bonds and often form gregarious flocks (Evans 2001; Seibert 2006). Inconsistent with environmental enrichment recommendations (discussed below; also see Bateson and Feenders 2010 and Schmidt 2010, both in this issue), laboratory confinement during research trials often requires solitary housing. However, it is probably uncommon that parrots are actively involved in trials for the duration of their laboratory confinement and more likely that trials account for only a small share of their time in laboratory housing. An ethical approach is to provide two types of enclosures, one that complies with the restrictive requirements of the experiment and another that accommodates expression of the animal’s natural behavior. Appropriate confinement construction and design should safeguard the health and well-being of both the birds and their caretakers. Depending on the nature and anticipated duration of the research project, it may be prudent to consider the use of resident animals at an off-site setting, such as a zoo or ornithological collection, instead of establishing on-site capacity in the research institution. Consideration of alternatives is particularly relevant in light of the substantial investments involved in the acquisition of birds, appropriate housing and daily care associated with the setup of an on-site parrot facility, and the discrepancy between the lifespan of the research subjects and the projected duration of research projects.

Table 2 Potential zoonotic diseases that can be contracted from contact with psittacine birds (adapted from Scott 2005)

Disease

Causal organism

Predominant route of transmission

Salmonellosis

Salmonella spp.

Orofecal

Subclinical to acute disease

Gastrointestinal signs, fever

Hygiene, RHCa

Psittacosis (ornithosis)

Chlamydophila psittaci

Inhalation

Subclinical to acute disease

Subclinical, respiratory signs (mortality)

Screening, hygiene, RHC

Yersiniosis

Y. pseudotuberculosis, Y. enterocolitica

Orofecal

Subclinical to acute disease

Gastrointestinal signs

Hygiene, rodent control

Tuberculosis

Mycobacterium spp.

Orofecal

Cutaneous lesions, systemic lesions

Local lesions, respiratory signs, urinary tract disorders

Hygiene, RHC

Ectoparasite infestation

Dermanyssus gallinae

Contact

Subclinical, pruritus, anemia

Pruritus, skin lesions

Hygiene, RHC

aRHC,

416

Effect on host Bird

Human

Control measures

routine health checks

ILAR Journal

Environmental Conditions Parrots require a circadian light-dark schedule, in which the dark period should be of adequate duration (about 12 hours) and without disruptions to facilitate sleep; an inappropriate photoperiod (i.e., a dark period that is either too long or too short) or poor night’s rest adversely affects their physical and emotional health (Bergman and Reinisch 2006; Lightfoot and Nacewicz 2006). The lighting schedule in animal rooms for parrots should try to mimic their natural habitat, with a yearround day length of 12 hours and a gradual transition between darkness and light (Dilger 1982b; Wilson 2005). Some birds (e.g., chickens) experience low-frequency light as stroboscopic (Nuboer et al. 1992; Prescott et al. 2003). Other environmental considerations include temperature, humidity, and noise levels. Extreme temperatures and high relative humidity should be avoided, although parrots tolerate a relatively wide range of these environmental parameters (Dilger 1982a). During the daytime parrots, which are noisy, gregarious animals themselves, are surrounded by noise in their natural habitat (complete silence often indicates the presence of a predator), but if the environment is too noisy, it can render the birds nervous or even noisier (Davis 1999). The provision of soft background music can help avoid continuous apprehensive states in parrots (Evans 2001). Type of Enclosure There are several options for bird housing: cage or aviary, solitary or nonsolitary, and indoor or outdoor. Each type has advantages and limitations. A cage is a relatively small enclosure for solitary or pair housing, whereas an aviary is a large, most often outdoor enclosure that can accommodate a flock of birds. Solitary housing is inadvisable because of the social nature of most parrot species (see the section below on Environmental Enrichment), but group housing can give rise to intraspecies aggression and so requires careful monitoring (Romagnano 2006). Indoor housing is usually more constraining in dimension, but outdoor housing increases the risk of infectious diseases contracted from wild birds (Lightfoot and Nacewicz 2006). Wilson (2006) advises not housing species that originated on different continents in the same airspace. Outdoor confinement offers the advantage of full-spectrum sunlight, through which ultraviolet B radiation enables endogenous vitamin D3 synthesis and thus promotes calcium metabolism (Stanford 2006; Wilson 2006). However, challenges inherent in such housing include higher risks of escape attempts by the birds and theft of the animals. Dimensions and Shape Scientifically based recommendations for species-specific cage dimensions are scarce. Enclosures should at least enable the birds to spread their wings and turn around while perched without touching the cage floor or walls with their tail or wings. Larger birds, long-tailed birds, or a greater number of Volume 51, Number 4

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birds require bigger enclosures (Dilger 1982a; Lightfoot and Nacewicz 2006; Turner 1992). The appropriateness of cage dimensions is determined by volume and shape, and both in turn dictate the number and kind of birds within. To facilitate flight, cages should be rectangular in shape and of sufficient length (and width) to accommodate airborne movement (Hawkins 2001; Luescher and Wilson 2006). Design The internal design and complexity of an enclosure are highly relevant to the birds’ usable space and comfort. Appropriate perches are a must in a psittacine enclosure (for a review of the advantages and disadvantages of different types of perches, Kalmar et al. 2007a). Favorable perch traits include good grip texture and suitable diameter (to ensure secure footing), flexibility (to stimulate balance and exercise), and varying diameter (to promote foot health); ideal perches are also chewable (environmental enrichment), nonslippery and not cold (in contrast to aluminum bars, for example), nonabrasive, and nontoxic (Kalmar et al. 2007a). Parrots are prey animals that roost in trees and the height of perches is important to ensure their sense of safety and comfort. As a general guideline, perch height should approximate human shoulder height (i.e., by suspending or elevating the enclosure) (Luescher and Wilson 2006; Wilson 2006). Other measures to promote a sense of security in parrots include the provision of a hiding place (e.g., a dark, cavitylike wooden box) or visual barriers in, on top of, or adjacent to the cage (Evans 2001). To provide clambering opportunities, the enclosure should have horizontal bars or mesh wire (Hawkins 2001); solid cage sides and vertical bars are definitely discouraged. Cage Position When positioning cages in an animal room, one should keep in mind that parrots are a prey species, so a preferred position is next to an opaque wall and/or away from doors or windows as the sudden passage of humans or vehicles outside the latter could startle the animal (Dilger 1982a; Evans 2001; Wilson 2005). There should be sufficient space or double wiring between enclosures to prevent birds from biting the toes of adjacently housed conspecifics (HarcourtBrown 2000; Stoodley et al. 1992). Large, adjacent hanging cages should allow easy passage along at least two free ends of the cages: the passage at the front side of the cages should be kept clear and used for daily husbandry procedures; the rear end of the cages ideally offers a protective barrier (e.g., through dense plant covering), with access only for facilitating nonroutine procedures such as capture of the birds. Accessibility and Safety Wide door-like openings should permit easy access to all corners of the cage through which the birds as well as all enclosure 417

items can be reached (Luescher and Wilson 2006). But water and feeding bowls should be easily accessible without the need to enter or open the enclosure (Luescher and Wilson 2006). The same is true for solid cage bottoms, for which drawer-like designs facilitate removal for cleaning and disinfection (Kalmar et al. 2007a,b). In hanging cages or aviaries, a mesh bottom enables removal of excrement and food spillage with minimal disturbance to the birds. These features also minimize the risk to animal caretakers of being bitten by the parrots, which can inflict serious flesh wounds. Because animal research often requires manual restraint, cage design and accessibility, coupled with personnel training in proper handling and catching techniques, can minimize stress and risk of injury to both the birds and the animal caretakers. Literature on techniques to manually restrain parrots is available (Kalmar et al. 2007a; Schulte and Rupley 2004). Materials used to construct cages must be noncorrosive and nontoxic. Galvanized wire cages have to be washed with diluted acetic acid and thoroughly brushed to remove all “white rust” (lumps of oxidized zinc) before use in order to prevent “new wire disease,” a form of zinc poisoning (Harcourt-Brown 2000; Howard 1992). Species-Specific Considerations Species-specific characteristics must be taken into account in all types of laboratory confinement. For example, certain parrot species are considerably more prone to aggressive behavior toward conspecifics than others. Male cockatoos in particular, but also macaws and Amazons, often inflict serious mate trauma when housed in pairs, although this apparently does not occur in free-ranging specimens (Romagnano 2006). Another example of a species-specific behavior applies to a minority of parrot species (e.g., many cockatoo species) that spend much of their active time in terrestrial activity (Wilson 2006). Cockatiels, for instance, normally display a distinctive running behavior; suspended wire cages are therefore discouraged for this species in favor of standing aviaries or cages with a solid (but not slippery or abrasive) bottom (Dilger 1982a; Hawkins 2001; Wilson 2006).

Environmental Enrichment Free-ranging parrots are accustomed to an environment in which they have been evolving for centuries and where they have developed a behavioral repertoire whose contextappropriate expression increases their chances of survival and reproduction. Psittacine species have been reported to forage for 4 to 6 hours per day (Snyder et al. 1987) and to spend most of their active time in close proximity to conspecifics. They typically move about the canopy or between shelters in open woodland areas to be less conspicuous to predators and have a considerable amount of control over their environment and the diversity of stimuli. When such birds, which as mentioned above are largely undomesticated, are housed in 418

environments that lack resemblance to their natural living conditions, they face a number of challenges. Constraints on the Expression of Species-Specific Behavior In captivity, parrots are often deprived of social contact and have limited opportunities for exploration and foraging. The latter is the appetitive phase of feeding behavior and precedes actual consumption of food (the consummatory phase). Under natural conditions, time spent performing behaviors from the appetitive phase amounts to several hours per day whereas in captivity, when “free food” is provided in a dish, the time involved in this activity decreases substantially (e.g., 30-72 min per day for orange-winged Amazon parrots), thereby decreasing the overall time spent feeding (reviewed in Meehan et al. 2003b). Furthermore, the reduction in (or even omission of) the appetitive phase reduces the diversity of the parrots’ behavioral repertoire, as does the restricted space available in enclosures, which limits the opportunity for locomotory behaviors. The constraint of these and other highly motivated behaviors may lead to frustration, which after prolonged exposure, unless the animal adapts, becomes chronic stress (Ödberg 1978) and can lead to the development of abnormal behaviors such as stereotypies (invariant, apparently useless behaviors that are repeated regularly over time; Ödberg 1978). There is much debate, however, about whether a stereotypy is an adaptive response (i.e., a means to cope with the stress caused by the limited environment) or a pathological manifestation (Mason 2006). Inanimate versus Animate Environmental Enrichment It has long been accepted that every effort should be made to enhance the quality of life for laboratory animals by reducing the stresses of a stimulus-poor environment (NRC 1996). One broad definition of 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” (Shepherdson et al. 1998). And for parrots, too, notwithstanding the limitations inherent in the captive confinement of psittacine species, behavioral research has shown that environmental enrichment is effective in preventing the development of abnormal repetitive behaviors (Lumeij and Hommers 2008; Meehan et al. 2003b). Enrichment for psittacines typically falls into inanimate and animate categories (for reviews, Evans 2001; Kalmar et al. 2007a; Meehan and Mench 2006). Inanimate enrichment comprises (1) adaptations to the physical cage environment (e.g., a swinging ladder, suspended plastic coil, or cotton rope wound around a spiral ring, for balancing, manipulating, and climbing exercises), (2) provision of manipulanda (e.g., objects and toys that can be manipulated with the beak and feet), and (3) foraging opportunities (e.g., items to prolong the appetitive phase of feeding such as barriers to chew ILAR Journal

through, food puzzles, and other containers that require the bird’s manipulation to obtain the food) (Meehan and Mench 2006). Animate enrichment includes social contact with both conspecifics and humans.6 Social parrot species, such as orange-winged Amazons, display differences in behavior when housed as same-sex pairs compared to their counterparts in solitary housing (Meehan et al. 2003a). The pair-housed birds more frequently made use of inanimate enrichment devices, were less fearful of novelty (inanimate and animate), spent less time screaming, and remained more active. More importantly, they did not develop any stereotypy throughout the 12month study. They did, however, show mild aggression toward one another (it was never severe enough to necessitate separation of pairs). Intraspecific aggression usually develops at the age of sexual maturity (Carpenter et al. 2001; Romagnano 2006) (between the ages of 4 and 6 years in Amazons), whereas the birds in the study of Meehan and colleagues (2003a) were only 2½ years old at the end of the experiment. With respect to interaction with humans, another study on orange-winged Amazons showed that, without access to inanimate enrichment in their home cage, they were more motivated to interact with humans (Meehan and Mench 2002).

teristics of the individual animal before implementing environmental enrichment, as long as individual accommodations do not interfere with experimental standardization. A fourth approach to environmental enrichment draws on the idea that laboratory animals lack appropriate challenges. A recent theoretical framework states that presenting animals with problems that are potentially stressful but which they possess the capacity to resolve may have a positive effect on behavioral and physiological animal welfare indicators (Meehan and Mench 2007). Of course, the challenge should be carefully designed to ensure that the animal is indeed able to solve the problem. In human-animal social interaction, challenges may be introduced to the bird through training sessions in which the animal masters a behavioral task (Pepperberg 2007). Last, after implementing an enrichment scheme, it is important to thoroughly evaluate its ergonomic costs to animal caretakers (e.g., additional cleaning of enrichment objects), its effectiveness with regards to the intended goals for the animals, and potential undesired side effects, and to make adaptations accordingly.

Fear-Minimizing Strategies Effectiveness of Environmental Enrichment The development of enrichment schemes requires consideration of a number of elements. First, enrichment objects with biological relevance will be most successful at stimulating behaviors from the species-specific ethogram. In orangewinged Amazons, for instance, researchers discovered that the color and hardness of preferred enrichment objects were similar to those of preferred food objects (Kim et al. 2009). More recently, research showed that in the same species, certain characteristics of manipulanda (rope) were preferred if they allowed expression of biologically relevant behavior (preening), although this effect depended on gender (Webb et al. 2010). Second, novel objects may not only stimulate exploration but also induce avoidance due to neophobia, both of which are somewhat related to psittacine habitat and diet characteristics (Mettke-Hofmann et al. 2002). Third, environmental enrichment in young parrots can reduce the likelihood of neophobia at a later age (Fox and Millam 2007). The degree of neophobia in juveniles is not necessarily constant as hand-raised birds showed decreased neophobia at 7 months, but similar levels of neophobia compared to parent-reared birds at 12 months (Fox and Millam 2004). Rotating the enrichment objects increases their efficiency, but individual differences modulate this effect: Fox and Millam (2007) demonstrated an increase in neophobia in the most fearful individuals of a colony of Amazons in response to frequent change of enrichment objects, whereas the opposite was true for less fearful individuals. For this reason it may be useful to take into account the behavioral charac6However,

introducing social contact for species that are known to be solitary, such as adult kakapos, may abolish the beneficial effects of environmental enrichment (Diamond et al. 2006).

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Efforts to adapt parrots’ physical environment should include consideration of fear-minimizing strategies. Captive birds cannot escape when they are exposed to unpleasant stimuli, which may not be perceived as such by their human handlers and/or caretakers. It is therefore advisable to provide some type of refuge in the cage or at least respect the safety of a sheltered cage wall, so the bird can learn that staying close to that wall gives it some control over the degree of stimulus exposure. It could be argued that providing shelter may decrease habituation to humans and thus complicate animal handling during experimentation. To our knowledge, this has not been systematically investigated in parrots used for research purposes, but conflicting evidence exists in other laboratory animal species (e.g., mice) (Hess et al. 2008; Moons et al. 2004).

Indications of Distress and Compromised Welfare Excessive Vocalization Almost all psittacine species are highly social and flockdwelling animals, displaying a wide variety of vocalizations— calm contact calls, loud alarm calls, food-begging calls, and interspecific agonistic calls—that help to promote flock cohesion (Bergman and Reinisch 2006). Vocalization is thus an inherent component of the normal repertoire of parrot behavior. It may become excessive in both loudness and frequency, and humans often consider any loud vocalization in parrots undesirable, excessive, or abnormal. But while such vocalizations may indicate disturbed well-being, they may also simply reflect unintentionally learned attention-seeking behavior. 419

It is important to try to distinguish between normal, distress-signaling, and learned vocalization in parrots. The underlying motivation should be considered by taking into account both the animals and elements in their environment. Normal vocalization is displayed according to a daily pattern that includes extensive morning and evening vocalization as well as several 15- to 20-minute loud vocalizations throughout the day (Wilson 2005). In contrast, prolonged and repetitive screaming, especially if it occurs throughout the day, may indicate boredom, alarm and fear (Alderton 2001; Davis 1991), a welfare concern related to a distressing environment, or, as mentioned, a desire for increased attention from caretakers (Bergman and Reinisch 2006).

Fear Behavior Fear is generally considered an unpleasant emotional state (Jones 1997), so animal caretakers and research personnel should be able to readily recognize species-specific signs of it. Parrots’ fear of humans is often directed at the hands; human faces rarely elicit fear reactions, but if the sight or proximity of a friendly face does provoke fear, it could indicate extreme fright (Wilson 2007). As parrots are prey animals, they may respond to fear by biting (Welle and Luescher 2006); more often, however, they instinctively attempt to avoid the threat by flying away (although panic flights can cause them injury). Other fear-induced behaviors include reluctance to approach (novel objects, humans, conspecifics), withdrawal, hiding, or alarm calls. If such signals are ignored, the animal may express stronger responses, such as fearful vocalization or a passive-aggressive posture (i.e., erection of all contour feathers) (Welle and Luescher 2006; Wilson 2007). As a last resort, the animal may bite, which usually leads to the desired outcome: cessation of interaction with the handler. Repetitive exposure to fearful situations in which humans ignore a bird’s warning signals increases the risk of apparently impulsive fear biting (Welle and Luescher 2006; Wilson 2006). In general, all sources of fear should be kept to a minimum and causal factors of seemingly unfounded dread actively be sought, followed by an attempt to overcome or minimize them. As discussed above, the use of diverse environmental enrichment strategies can reduce the likelihood of fear responses. Several standardized methods are available to objectively evaluate the level of fear in parrots. For instance, it is possible to assess an animal’s fear toward a novel object by measuring its latency to feed on a highly favored food item in the presence of the object (Mettke-Hofmann et al. 2002). A second test measures both the latency of first contact with a novel object and the duration of interaction within a fixed time interval (Meehan and Mench 2002; Mettke-Hofmann et al. 2002); a longer latency does not necessarily reflect greater fear, however, but may indicate a low motivation for exploration, which is likely if the duration of interaction is also low (Meehan and Mench 2002). A third method to test fear toward a novel object is to introduce it to the parrot in a familiar environment— for example, by placing or hanging it in the home cage—and 420

evaluate the animal’s behavior, proximity to the object, and bite marks resulting from manipulation (Fox and Millam 2004). Assessments of fear toward familiar or unfamiliar people involve a handler response test that scores birds’ reactions (e.g., flight distance, bites, screams) to the following stimuli: extending a finger toward the bird, touching the bird on different parts of the body, offering food, and standing or sitting near the bird (Meehan and Mench 2002).

Abnormal Repetitive Behavior According to Garner (2007) abnormal repetitive behaviors are those that “are inappropriately repetitive in goal or motor pattern, and are functionless, maladaptive, or self-injurious.” They comprise stereotypies and impulsive/compulsive behaviors (e.g., feather picking; for review, Van Zeeland et al. 2009). Meehan and Mench (2006) classify parrot stereotypies into three main categories: (1) locomotor (e.g., route tracing, pacing, corner flipping), (2) oral (e.g., spot pecking, sham chewing, bar biting, tongue rolling), and (3) objectdirected (repetitive, invariant manipulation of objects). In rare cases, parrots have been known to develop vocal stereotypies (screaming) (Bergman and Reinisch 2006). The development of a stereotypy is often linked to frustration caused by constraint of a highly motivated behavior (Mason 1991; Meehan and Mench 2006). The stereotypic behavior can become disengaged from its original cause and continue to be performed even after environmental conditions are improved, and may thus not necessarily indicate currently compromised welfare but rather provide information about the animal’s history. Conditions known to elicit stereotypic behavior in parrots include impaired foraging opportunities, insufficient opportunity for locomotion, and lack of (physical) social contact with conspecifics (Meehan et al. 2003a, 2004; Meehan and Mench 2006). Meehan and colleagues (2004) demonstrated that environmental enrichment in the form of foraging opportunities and increased level of cage complexity significantly reduced—but did not completely eliminate—the performance of stereotypies in single-housed Amazons. In pair-housed Amazons, however, the same environmental enrichment protocol completely inhibited development of stereotypies (Meehan et al. 2003a).

Disease A healthy bird colony requires quarantine units, separate housing and infectious disease monitoring for newly acquired birds, and thorough health checks of all birds at regular intervals. Aside from obvious signs of trauma or infectious disease, animal care and research personnel should also be attentive to more subtle indications of impaired health (including malnutrition), such as abnormal plumage,7 bone dimorphism, emaciation, clinical signs of metabolic disease, 7Examples

of abnormal plumage are stress bars, weakened feathers, broken or damaged feathers, and depigmentation (reviewed in Koski 2002).

ILAR Journal

or infectious disease resulting from impaired immunological function. Inadequate management or housing conditions, such as abrasive perches, suboptimal environmental temperature, or unsatisfactory hygiene, can also lead to lesions or other indications of impaired health. Most diseases and conditions are accompanied by discomfort, distress, and eventually severe pain or even death. Animal caretakers and research personnel should therefore carefully monitor all individual birds on a regular basis, actively looking for signs of compromised health, which are often subtle and go unnoticed to the inattentive eye. These precautions are necessary to protect both the animals’ welfare and the quality of the research data. The experimental use of healthy animals may reduce interindividual variability and improve the statistical power of experimental designs (Garner 2005), thus reducing—or at least not unnecessarily increasing—the number of animal trials and animal numbers.

Conclusions We have reviewed the current state of knowledge for the housing and management of Psittaciformes as laboratory animals. Because parrots are long-lived, highly intelligent, and largely nondomesticated, their confinement in laboratory settings requires careful thought and long-term planning as well as consideration of environmental enrichment and fear-minimizing strategies. With the exception of a number of scientifically based studies on inanimate and animate enrichment, research data on species-specific housing guidelines for parrots are quite scarce. Researchers should acquaint themselves with a wide variety of aspects of parrot husbandry in order to be sufficiently knowledgeable to make sound decisions about acquisition, husbandry conditions, and potential health and welfare issues.

Acknowledgments Aagje Veys and Sofie Merciny are kindly acknowledged for their constructive comments.

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