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 (behav-
ior, acoustics, and vision; 17%). Confinement of psittacine
species for research purposes is a matter of concern as scien-
tifically based species-specific housing guidelines are scarce.
The aim of this article is to provide scientific information rel-
evant to the laboratory confinement of Psittaciformes to pro-
mote the refinement of acquisition, housing, and maintenance
practices of these birds as laboratory animals. We briefly dis-
cuss 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 domestica-
tion status) and psittacine cognition. We then discuss consider-
ations in the acquisition of laboratory parrots and review
important management issues such as nutrition, zoonoses,
housing, and environmental enrichment. The final section re-
views 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 isabelle.kalmar@ugent.be.
Volume 51, Number 4 2010
most popular companion animal, estimated at 10.1 million
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individuals in 2002 (AVMA 2002). Although their confine-
ment 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 Labora-
tory and Other Research Animals (UFAW 2010), a labora-
tory animal in the broadest sense is “any non-human member
of the animal kingdom which is kept in captivity for experi-
mental 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, hema-
tology, 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 indi-
viduals 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 underrepre-
sentation 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 off-
site facilities, and for 35% of cases (n = 11) housing infor-
mation 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 BS EC GEN NUTR Total (%)

Field study 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%)
Undetermined 8 0 1 2 0 11 (8%)

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Total 63 24 33 18 3 141 (100%)

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) Background Information

used individual housing, 13% (n = 4) pair housing, and 29%
(n = 9) group housing.
The aim of this article is to provide scientific informa-
tion concerning laboratory confinement of Psittaciformes,
with the intention of refining arrangements for their acqui-
sition, housing, and maintenance. We begin with an over-
view of systematics, geographic distribution, and specific
legislation and conservation status. The next section pres-
ents 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 compro-
mised welfare.
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. Tradition-
ally, 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 cen-
triole 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 ILAR Journal

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 plum-
age). 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. meridio-
nalis). 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 anatom-
ical 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 Austra-
lia 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 (Loricu-
lus spp.) and ring-necked parakeets (Psittacula spp.). Pionus
parrots (Pionus spp.), macaws (e.g., Ara, Cyanopsitta, and An-
odorhynchus spp.) and conures (e.g., Aratinga, Cyanoliseus,
and Pyrrhura spp.) are native to South America, and the Ama-
zons (Amazona spp.) originate from Central and South Amer-
ica. 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 indige-
nous to Australia (Russell 1987).
Irrespective of geographical origin, descendants of es-
caped 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 popula-
tions 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 self-
sustaining 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 caro-
lensis) and the thick-billed parrot (Rhynchopsitta pachy-
rhyncha), disappeared during the 20th century (Butler 2005).
Although efforts to reestablish the latter have not resulted in
self-sustaining wild populations, release experiments with
1Blue feather color is formed by nanostructures in the feather called Dyck
texture (Dyck 1971a,b).
Volume 51, Number 4 2010
wild-caught birds from Mexico, where the species is still
extant, have resulted in a limited number of surviving, trans-
located 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 Endan-
gered Species (CITES2), an international treaty that classifies
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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 ex-
tinction 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 Appen-
dix II (CITES 2009). Only four species of Psittaciformes are
not considered at risk: peach-faced lovebirds (Agapornis ro-
seicollis), budgerigars (Melopsittacus undulatus), cockatiels
(Nymphicus hollandicus), and rose-ringed parakeets (Psit-
tacula 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 ver-
tebrate animal use in research, teaching, or testing is consid-
ered 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 orig-
inal 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 explic-
itly excludes birds bred for research (Cohen 2006). US re-
search 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 manage-
ment.3 In contrast to US guidelines and restrictions, Euro-
pean 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
3The recent update of the Guide (8th ed., NRC 2010) includes references for
readers interested in this information for birds.
411
pain, suffering, distress, or lasting harm as animal experi-
ments (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). Im-
port or export of Appendix I specimens is allowed under
very strict permitting requirements only for scientific pur-
poses, 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 (Eu-
ropean 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, importa-
tion of CITES-listed avians (with some exceptions, includ-
ing 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 diag-
nosed 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 ex-
otic 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 Ro-
mans. 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 repro-
ductive 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 im-
provement in captive breeding was the development of endo-
scopic 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 cap-
tivity (Crosta et al. 2002; Gartrell 2002; Harcourt-Brown
2000; Silva 1991).
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Yet domestication—the process of adaptation to captiv-
ity through genetic changes—is still in its infancy for parrots
and other psittacines (Meehan et al. 2003b). Although par-
rots 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 con-
sidered wild animals (with the possible exceptions of bud-
gerigars 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 un-
dergone selection for behavioral traits that facilitate adapta-
tion 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, espe-
cially 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 ne-
cessitate careful consideration of the choice of species and
housing conditions. Parrots’ vocalizations, and especially
their ability to mimic the human voice, are a distinctive man-
ifestation 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 (Psit-
tacula 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 fission-
fusion 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 Afri-
can 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 in-
cluded 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 spon-
taneous categorization into unlabeled edible or nonedible
items (Giret et al. 2009; Pepperberg 1995). Although most
cognitive research in parrots has involved African grey par-
rots, 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 spe-
cies (two macaw and one Amazon species).
The cognition of parrots is consistent with several char-
acteristics generally associated with advanced cognitive pro-
cessing, such as a relatively large brain, slow development,
longevity, and a long period of parental association (Shuck-
Paim and Borsari 2009).
Factors to Consider in the Selection of
Laboratory Parrots
The acquisition of animals that will be confined in labora-
tory 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, back-
ground, 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 cogni-
tively developed species should be the species of choice con-
sistent with achieving the experimental goals.
In addition, several other factors are important to con-
sider. 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 pos-
sibly require the use of additional animals). Second, good
knowledge of the animals’ background improves interpreta-
tion of research data and promotes sound decisions on nec-
essary 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 socializa-
tion of birds is of utmost importance in their laboratory
confinement. Socialization facilitates handling by animal
Volume 51, Number 4 2010
caretakers, enhances the performance of experimental pro-
cedures, 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 labora-
tory 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 deleteri-
ous to the well-being of certain species. Further, the loudness
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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 hous-
ing 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 rela-
tively 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 partic-
ular 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 mo-
bilization 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 labo-
ratory 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 ad-
versely affect animal health and welfare as well as experi-
mental 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 nat-
ural 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 spe-
cies 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, physi-
cal constraints would hamper wild parrots’ foraging on pea-
nuts 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 pig-
ments, 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 struc-
tural color and endogenously produced yellow pigments
(Dyck 1971a,b; McGraw and Nogare 2005; Rowley 1997).
Black, brown, and grey shades result from melanin pigmen-
tation, 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 con-
tain 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 pro-
vision of additional sodium and other minerals when the di-
etary 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 vita-
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mins, and contain a deteriorated calcium:phosphorus ratio (e.g.,
Harrison 1998; Ullrey et al. 1991; Wolf et al. 1998). Manifesta-
tion 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 pre-
sented to veterinarians (Harrison 1998).
In addition, because parrots dehusk seeds (thereby con-
suming only the kernel) and display a profoundly selective
feeding behavior when provided a multicomponent diet, pre-
ferring 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) in-
corporated in these seed-based diets (Kalmar et al. 2010).
Nutritional supplementation through drinking water is
not recommended as vitamins are unstable in aqueous solu-
tions and reduce water palatability, possibly decreasing wa-
ter intake and introducing a risk of dehydration (Donoghue
and Stahl 1997; Hawley 1997).
Pellet Diets: Advantages
Pellet diets rather than seed mixtures are strongly recom-
mended for birds used in laboratory research because they
offer two important advantages: they prevent selective feed-
ing 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 multi-
component diet, management and/or animal factors may re-
sult 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 inac-
curate 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 with-
out 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 bar-
ren 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. Con-
version 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 le-
sions in other granivorous birds (i.e., chickens; Bird et al.
1937) raised concerns that the same might be true for par-
rots. 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 sim-
ply 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 specializa-
tions. 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).
Volume 51, Number 4 2010
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 necta-
rivorous 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 di-
luted before use; the degree of dilution affects voluntary intake
and thus energy and nutrient supply (Kalmar et al. 2009).
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Food Storage
The method of storage can vastly alter the nutritional com-
position of the manufacturer’s formulation because food is
often stored in large containers in which different-sized in-
gredients segregate. It is therefore advisable to regularly stir
the food and completely empty storage containers of multi-
component diets before refilling to ensure that all compo-
nents are eventually fed to the animals. An alternative option
is to store food in the original bags (Kalmar et al. 2010), al-
though closed feed containers offer the advantage of im-
proved protection against vermin.
Food should be properly stored and consumed (or dis-
posed of) by the manufacturer’s indicated date, as improper
(i.e., suboptimal temperature or relative humidity) or pro-
longed storage can promote the formation of mycotoxins
(Samour 2004). Exposure to air or light also negatively af-
fects the nutritional quality of foods, for example by reducing
the content of several vitamins (Reddy and Love 1999). Ac-
cording to Bavelaar and Beynen (2003), oxidation of polyun-
saturated 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 di-
rectly from psittacine birds or indirectly from their excreta
or contaminated materials and air. Adequate personal and
environmental hygiene measures—including vermin con-
trol, 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
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 pro-
vides a partial list of zoonotic agents that can be con-
tracted 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
Housing
Despite their widespread geographic distribution, most par-
rot 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 envi-
ronmental enrichment recommendations (discussed below;
also see Bateson and Feenders 2010 and Schmidt 2010, both

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ornithosis). Parrots can be asymptomatic carriers and shed-
ders of chlamydiosis, and the strains found in Amazon par-
rots 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 (yel-
low to green urates), and oculonasal discharge (Gould 1995;
Greenacre 2003; Turner 1987). In humans the infection usu-
ally also passes subclinically, but clinical signs may vary
from mild respiratory disease to pneumonia, nausea, vomit-
ing, hepatitis, myocarditis, disorientation, mental depres-
sion, delirium, and even death. Possible transmission routes
of C. psittaci from birds to humans include, in order of im-
portance, inhalation of contaminated air; direct contact with
birds, feathers, excreta, oculonasal discharge, or infected
tissue; and bites or other open wounds. The incubation pe-
riod 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 as-
say, but none of these has proven to be 100% accurate
(Gould 1995; Turner 1987).
in this issue), laboratory confinement during research trials
often requires solitary housing. However, it is probably un-
common 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 labora-
tory housing. An ethical approach is to provide two types of
enclosures, one that complies with the restrictive require-
ments of the experiment and another that accommodates ex-
pression 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 orni-
thological collection, instead of establishing on-site capacity
in the research institution. Consideration of alternatives is par-
ticularly relevant in light of the substantial investments in-
volved in the acquisition of birds, appropriate housing and
daily care associated with the setup of an on-site parrot facil-
ity, 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)

Predominant Effect on host

route of Control
Disease Causal organism transmission Bird Human measures

Salmonellosis Salmonella spp. Orofecal Subclinical to Gastrointestinal Hygiene, RHCa

acute disease signs, fever
Psittacosis Chlamydophila Inhalation Subclinical to Subclinical, respiratory Screening,
(ornithosis) psittaci acute disease signs (mortality) hygiene, RHC
Yersiniosis Y. pseudotuberculosis, Orofecal Subclinical to Gastrointestinal Hygiene, rodent
Y. enterocolitica acute disease signs control

Tuberculosis Mycobacterium spp. Orofecal Cutaneous lesions, Local lesions, Hygiene, RHC
systemic lesions respiratory signs,
urinary tract disorders
Ectoparasite Dermanyssus Contact Subclinical, pruritus, Pruritus, skin lesions Hygiene, RHC
infestation gallinae anemia

aRHC, routine health checks

416 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 year-
round 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 strobo-
scopic (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 pres-
ence 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, soli-
tary or nonsolitary, and indoor or outdoor. Each type has ad-
vantages 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 na-
ture of most parrot species (see the section below on Environ-
mental Enrichment), but group housing can give rise to
intraspecies aggression and so requires careful monitoring
(Romagnano 2006). Indoor housing is usually more constrain-
ing 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 endog-
enous vitamin D3 synthesis and thus promotes calcium me-
tabolism (Stanford 2006; Wilson 2006). However, challenges
inherent in such housing include higher risks of escape at-
tempts 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 2010
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
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highly relevant to the birds’ usable space and comfort. Ap-
propriate 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 exer-
cise), and varying diameter (to promote foot health); ideal
perches are also chewable (environmental enrichment), non-
slippery and not cold (in contrast to aluminum bars, for ex-
ample), 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 com-
fort. As a general guideline, perch height should approxi-
mate 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, cavity-
like wooden box) or visual barriers in, on top of, or adjacent
to the cage (Evans 2001). To provide clambering opportuni-
ties, the enclosure should have horizontal bars or mesh wire
(Hawkins 2001); solid cage sides and vertical bars are defi-
nitely discouraged.
Cage Position
When positioning cages in an animal room, one should keep
in mind that parrots are a prey species, so a preferred posi-
tion is next to an opaque wall and/or away from doors or
windows as the sudden passage of humans or vehicles out-
side 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 bit-
ing the toes of adjacently housed conspecifics (Harcourt-
Brown 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 facilitat-
ing nonroutine procedures such as capture of the birds.
Accessibility and Safety
Wide door-like openings should permit easy access to all cor-
ners 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 disin-
fection (Kalmar et al. 2007a,b). In hanging cages or aviaries,
a mesh bottom enables removal of excrement and food spill-
age 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. Lit-
erature 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 fa-
vor of standing aviaries or cages with a solid (but not slip-
pery 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 context-
appropriate 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 environ-
ment 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 lat-
ter is the appetitive phase of feeding behavior and precedes ac-
tual consumption of food (the consummatory phase). Under
natural conditions, time spent performing behaviors from the
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appetitive phase amounts to several hours per day whereas in
captivity, when “free food” is provided in a dish, the time in-
volved in this activity decreases substantially (e.g., 30-72 min
per day for orange-winged Amazon parrots), thereby decreas-
ing 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 stereo-
typies (invariant, apparently useless behaviors that are repeated
regularly over time; Ödberg 1978). There is much debate, how-
ever, about whether a stereotypy is an adaptive response (i.e., a
means to cope with the stress caused by the limited environ-
ment) 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 reduc-
ing 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 envi-
ronmental 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 re-
search has shown that environmental enrichment is effective
in preventing the development of abnormal repetitive behav-
iors (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, manipulat-
ing, 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 pro-
long 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 impor-
tantly, they did not develop any stereotypy throughout the 12-
month 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 in-
animate enrichment in their home cage, they were more mo-
tivated to interact with humans (Meehan and Mench 2002).
Effectiveness of Environmental Enrichment
The development of enrichment schemes requires consider-
ation of a number of elements. First, enrichment objects with
biological relevance will be most successful at stimulating
behaviors from the species-specific ethogram. In orange-
winged 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, cer-
tain 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, en-
vironmental 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 necessar-
ily constant as hand-raised birds showed decreased neopho-
bia 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 charac-
6However, 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).
Volume 51, Number 4 2010
teristics of the individual animal before implementing envi-
ronmental 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 pos-
sess the capacity to resolve may have a positive effect on behav-
ioral 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
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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 im-
portant 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
Efforts to adapt parrots’ physical environment should in-
clude 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 pro-
vide 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 de-
gree of stimulus exposure. It could be argued that providing
shelter may decrease habituation to humans and thus com-
plicate 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 flock-
dwelling 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 cohe-
sion (Bergman and Reinisch 2006). Vocalization is thus an
inherent component of the normal repertoire of parrot behav-
ior. 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 vocaliza-
tions 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 un-
derlying motivation should be considered by taking into ac-
count 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 through-
out the day (Wilson 2005). In contrast, prolonged and repeti-
tive 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 environ-
ment, 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; hu-
man faces rarely elicit fear reactions, but if the sight or prox-
imity 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 fac-
tors of seemingly unfounded dread actively be sought, fol-
lowed 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 pres-
ence 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 inter-
val (Meehan and Mench 2002; Mettke-Hofmann et al. 2002);
a longer latency does not necessarily reflect greater fear, how-
ever, 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 ob-
ject 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 peo-
ple 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 differ-
ent parts of the body, offering food, and standing or sitting
near the bird (Meehan and Mench 2002).
Abnormal Repetitive Behavior
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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 be-
haviors (e.g., feather picking; for review, Van Zeeland et al.
2009). Meehan and Mench (2006) classify parrot stereotyp-
ies into three main categories: (1) locomotor (e.g., route trac-
ing, pacing, corner flipping), (2) oral (e.g., spot pecking,
sham chewing, bar biting, tongue rolling), and (3) object-
directed (repetitive, invariant manipulation of objects). In
rare cases, parrots have been known to develop vocal stereo-
typies (screaming) (Bergman and Reinisch 2006).
The development of a stereotypy is often linked to frus-
tration 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 condi-
tions are improved, and may thus not necessarily indicate
currently compromised welfare but rather provide informa-
tion 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 enrich-
ment 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 in-
hibited development of stereotypies (Meehan et al. 2003a).
Disease
A healthy bird colony requires quarantine units, separate
housing and infectious disease monitoring for newly ac-
quired birds, and thorough health checks of all birds at regu-
lar 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 tem-
perature, or unsatisfactory hygiene, can also lead to lesions
or other indications of impaired health.
Most diseases and conditions are accompanied by dis-
comfort, distress, and eventually severe pain or even death.
Animal caretakers and research personnel should therefore
carefully monitor all individual birds on a regular basis, ac-
tively 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’ wel-
fare and the quality of the research data. The experimental
use of healthy animals may reduce interindividual variabil-
ity and improve the statistical power of experimental
designs (Garner 2005), thus reducing—or at least not un-
necessarily 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 labora-
tory 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 en-
richment, research data on species-specific housing guide-
lines for parrots are quite scarce. Researchers should acquaint
themselves with a wide variety of aspects of parrot hus-
bandry 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.
References
Alderton D. 2001. Kooi- en volièrevogels. Utrecht: Veltman Uitgevers.
ARENA [Applied Research and Ethics National Association]/OLAW
[Office of Laboratory Animal Welfare]. 2002. Institutional animal care
and use committee guidebook, 2nd ed. Bethesda: OLAW.
AAFCO [Association of American Feed Control Officials]. 1998. Nutrition
expert panel review: New rules for feeding pet birds. Feed Mgmt
49:23-25.
AVMA [American Veterinary Medical Association]. 2002. US Pet Owner-
ship and Demographics Sourcebook. Shaumburg: Center for Informa-
tion Management.
Bateson M, Feenders G. 2010. The use of passerine bird species in labora-
tory research: Implications of basic biology for husbandry and welfare.
ILAR J 51:394-408.
Bavelaar FJ, Beynen AC. 2003. Qualification of commercial feeds for
parrots. Tijdschr Diergeneesk 128:726-734.
Volume 51, Number 4 2010
Bergman L, Reinisch US. 2006. Parrot vocalisation. In: Luescher AU,
ed. Manual of Parrot Behaviour. Oxford: Blackwell Publishing.
p 219-223.
Bird HR, Oleson JJ, Elvehjem CA, Hart EB. 1937. Relation of grit to the
development of the gizzard lining in chicks. Poultry Sci 16:238-242.
Brightsmith DJ, Muñoz-Najar RA. 2004. Avian geophagy and soil charac-
teristics in Southeastern Peru. Biotropica 36:534-543.
Burger J. 2003. Parrot behaviour at a Rio Manu (Peru) clay lick: Temporal
patterns, associations, and antipredator responses. Acta Ethol 6:23-34.
Butler CJ. 2005. Feral parrots in the continental United States and United
Kingdom: Past, present and future. J Avian Med Surg 19:142-149.
Cannon CE. 1984. The diet of lorikeets Trichoglossus spp. in the Queensland-
New South Wales border region. Emu 84:16-22.
Downloaded from https://academic.oup.com/ilarjournal/article-abstract/51/4/409/676068 by guest on 17 November 2019
Carpenter JW, Mashima TY, Rupiper DJ. 2001. Exotic Animal Formulary,
2nd ed. Philadelphia: WB Saunders.
CITES. 1973. Convention on International Trade in Endangered Species of
Wild Fauna and Flora. Available online (www.cites.org), accessed July
29, 2010.
CITES. 2009. Appendices I, II, and III. Available online (www.cites.org/
eng/app/appendices.shtml), accessed July 29, 2010.
Cohen H. 2006. The Animal Welfare Act. J Anim Law 2:13-26.
Collar NJ. 1997. Family Psittacidae (Parrots). In: del Hoyo J, Elliott A,
Sargatal J, eds. Handbook of the Birds in the World, vol 4. Barcelona:
Lynx Editions. p 280-477.
Cornejo J, Clubb S. 2005. Analysis of the maintenance diet offered to lories
and lorikeets (Psittaciformes; Loriinae) at Loro Parque Fundacion, Ten-
erife. Int Zoo Yb 39:85-98.
Crosta L, Gerlach H, Bürckle HM, Timossi L. 2002. Endoscopic testicular
biopsy technique in psittaciformes. J Avian Med Surg 16:106-110.
Davis CS. 1991. Parrot psychology and behavior problems. Vet Clin N Am
Sm Anim Pract 21:1281-1288.
Davis C. 1999. Basic considerations for avian behavior modification. Semin
Avian Exot Pet 8:183-195.
Diamond J, Bond AB. 1991. Social behaviour and the ontogeny of foraging
in the kea (Nestor notabilis). Ethology 88:128-144.
Diamond J, Eason D, Reid C, Bond AB. 2006. Social play in kakapo (Strig-
ops habroptilus) with comparisons to kea (Nestor notabilis) and kaka
(Nestor meridionalis). Behaviour 143:1397-1423.
Dilger WC. 1982a. Caging and environment. In: Petrak ML, ed. Diseases of
Cage and Aviary Birds, 2nd ed. Philadelphia: Lea and Febiger. p 11-17.
Dilger WC. 1982b. Behavioral aspects. In: Petrak ML, ed. Diseases of Cage
and Aviary Birds, 2nd ed. Philadelphia: Lea and Febiger. p 18-20.
Donoghue S, Stahl S. 1997. Clinical nutrition of companion birds. J Avian
Med Surg 11:228-246.
Dyck J. 1971a. Structure and spectral reflectance of green and blue feathers of
the rose-faced lovebird (Agapornis roseicollis). Biol Skrifter 18:1-67.
Dyck J. 1971b. Structure and color-production of the blue barbs of Aga-
pornis roseicollis and Cotinga maynana. Zeitschr für Zellforsch 115:
17-29.
Earle KE, Clarke NR. 1991. The nutrition of the budgerigar (Melopsittacus
undulatus). J Nutr 121:S186-S192.
Eason DK, Elliott GP, Merton DV, Jansen PW, Harper GA. 2006. Breeding
biology of kakapo Strigops habroptilus on offshore island sanctuaries
1990-2002. Notornis 5:27-36.
European Community. 1979. Council Directive 79/409 on the conservation
of wild birds. Official Journal of the European Communities. Luxem-
bourg: European Community (OJ L103).
European Community. 1986. Council Directive 86/609 on the approxima-
tion of laws, regulations and administrative provisions of the member
states regarding the protection of animals used for experimental and
other scientific purposes. Official Journal of the European Communi-
ties. Luxembourg: European Community (OJ L 358).
Evans M. 2001. Environmental enrichment for pet parrots. In Practice
23:596-605.
Federal Register. 2004. Animal Welfare: Regulations and standards for
birds, rats, and mice. FR 69:31537-31541.
Forshaw JM, Cooper WT. 1978. Parrots of the World, 2nd ed. London: Blan-
ford Press.
421
Forshaw JM, Cooper WT. 1989. Parrots of the World, 3rd ed. London: Blan-
ford Press.
Forshaw JM, Cooper WT. 2002. Australian Parrots, 3rd ed. Robina, Queens-
land: Alexander Editions.
Fox RA, Millam JR. 2004. The effect of early environment on neophobia in
orange-winged Amazon parrots. Appl Anim Behav Sci 89:117-129.
Fox RA, Millam JR. 2007. Novelty and individual differences influence
neophobia in orange-winged Amazon parrots (Amazona amazonica).
Appl Anim Behav Sci 104:107-115.
Garner JP. 2005. Stereotypies and other abnormal repetitive behaviors: Po-
tential impact on validity, reliability, and replicability of scientific out-
comes. ILAR J 46:106-117.
Garner JP. 2007. Perseveration and stereotypy: Systems-level insights from
clinical psychology. In: Rushen J, Mason G, eds. Stereotypic Animal
Behaviour: Fundamentals and Applications to Welfare. Wallingford:
CABI. p 232-152.
Gartrell BD. 2000. The nutritional, morphologic, and physiologic bases of
nectarivory in Australian birds. J Avian Med Surg 14:85-94.
Gartrell BD. 2002. Assessment of the reproductive state in male swift par-
rots (Lathamus discolour) by testicular aspiration and cytology. J Avian
Med Surg 16:211-217.
Ghysels P. 1997. Transferring birds to pellet feeding: Successful methods
for different species. Proc First Internat Symp Pet Bird Nutrition,
Hannover, October 3-4. p 98.
Gilardi JD, Sean SD, Munn CA, Tell LA. 1999. Biochemical functions of
geophagy in parrots: Detoxification of dietary toxins and cytoprotective
effects. J Chem Ecol 25:897-922.
Giret N, Péron F, Nagle L, Kreutzer M, Bovet D. 2009. Spontaneous catego-
rization of vocal imitations in African grey parrots (Psittacus erithacus).
Behav Proc 82:244-248.
Gould WJ. 1995. Common digestive tract disorders in pet birds. Vet Med-US
90:40-52.
Greenacre CB. 2003. The avian patient. In: Ballard B, Cheek R, eds. Exotic
Animal Medicine for the Veterinary Technician. Ames: Blackwell Pub-
lishing. p 5-30.
Harcourt-Brown NH. 2000. Psittacine birds. In: Tully TN, Lawton MCP,
Dorrestein GM, eds. Avian Medicine. Oxford: Butterworth. p 112-143.
Hargis AM. 1989. Avocado (Persea americana) intoxication in caged birds.
JAVMA 94:64-66.
Harrison GJ. 1998. Twenty years of progress in pet bird nutrition. JAVMA
212:1226-1230.
Hawkins P. 2001. Laboratory birds: Refinements in husbandry and proce-
dures. Lab Anim 35:S1-S163.
Hawley SB. 1997. Nutritional comparison of diets fed to pet birds. Proc
First Internat Symp Pet Bird Nutrition, Hannover, October 3-4. p 55.
Hess SE, Rohr S, Dufour BD, Gaskill BN, Pajor EA, Garner JP. 2008.
Home improvement: C57BL/6J mice given more naturalistic nesting
materials build better nests. JAALAS 47:25-31.
Houston D, Mcinnes K, Elliott G, Eason D, Moorhouse R, Cockrem J.
2007. The use of a nutritional supplement to improve egg production in
the endangered kakapo. Biol Conserv 138:248-255.
Howard BR. 1992. Health risks of housing small psittacines in galvanized
wiremesh cages. JAVMA 200:1667-1674.
Jamieson BG, Tripepi S. 2005. Ultrastructure of the spermatozoon of
Apus apus (Linnaeus 1758), the common swift (Aves; Apodiformes;
Apodidae), with phylogenetic implications. Acta Zool-Stockholm
86:239-244.
Jones RB. 1997. Fear and distress. In: Appleby MC, Hughes BO, eds. Ani-
mal Welfare. New York: CAB International. p 75-87.
Kalmar ID, Moons CPH, Meers LL, Janssens GPJ. 2007a. Psittacine birds
as laboratory animals: Refinements and assessment of welfare. JAALAS
46:8-15.
Kalmar ID, Werquin G, Janssens GPJ. 2007b. Apparent nutrient digestibil-
ity and excreta quality in African grey parrots fed two pelleted diets
based on coarsely or finely ground ingredients. J Anim Physiol An N
91:210-216.
Kalmar ID, van Loon M, Bürkle M, Reinschmidt M, Waugh D, Werquin G,
Janssens GPJ. 2009. Effect of dilution degree of commercial nectar and
422
provision of fruit on food, energy and nutrient intake in two rainbow
lorikeet subspecies. Zoo Biol 28:98-106.
Kalmar ID, Veys AC, Geeroms B, Reinschmidt M, Waugh D, Werquin G,
Janssens GPJ. 2010. Impact of additional fruit and segregation, seed
selection and seed dehusking of multi-component seed diets on volun-
tary nutrient and energy intake in yellow-shouldered Amazons
(Amazona barbadensis). J Anim Physiol An N, doi: 10.111/j.1439-
0396.2010.01026.x.
Kim LC, Garner JP, Millam JR. 2009. Preferences of orange-winged Ama-
zon parrots (Amazona Amazonica) for cage enrichment devices. Appl
Anim Behav Sci 120:216-223.
Kollias GV. 1995. Diets, feeding practices, and nutritional problems in psit-
tacine birds. Vet Med US 90:29-39.
Downloaded from https://academic.oup.com/ilarjournal/article-abstract/51/4/409/676068 by guest on 17 November 2019
Koski MA. 2002. Dermatologic diseases in psittacine birds: An investiga-
tional approach. Semin Avian Exot Pet 11:105-124.
Levine BL. 2003. Common disorders of Amazons, Australian parakeets,
and African grey parrots. Semin Avian Exot Pet 12:125-130.
Lightfoot T, Nacewicz CL. 2006. Psittacine behavior. In: Bays TB, Lightfoot
T, Mayer J, eds. Exotic Pet Behaviour. St. Louis: Saunders. p 51-101.
Luescher AU, Wilson L. 2006. Housing and management considerations for
problem prevention. In: Luescher AU, ed. Manual of Parrot Behaviour.
Oxford: Blackwell Publishing. p 291-299.
Lumeij TJ, Hommers CJ. 2008. Foraging “enrichment” as treatment for
pterotillomania. Appl Anim Behav Sci 111:85-94.
Marler P. 1970. A comparative approach to vocal learning: Song develop-
ment in white-crowned sparrows. J Comp Physiol Psych 71:1-25.
Mason GJ. 1991. Stereotypies: A critical review. Anim Behav 41:1015-1037.
Mason GJ. 2006. Stereotypic behaviour in captive animals: Fundamentals
and implications for welfare and beyond. In: Mason GJ, Rushen J, eds.
Stereotypic Animal Behaviour: Fundamentals and Applications to
Welfare, 2nd ed. Oxfordshire: CABI. p 325-356.
Matsunaga E, Okanoya K. 2009. Evolution and diversity in avian vocal sys-
tem: An evo-devo model from the morphological and behavioral per-
spectives. Devel Growth Differ 51:355-367.
McGraw KJ, Nogare MC. 2005. Distribution of unique red feather pigments
in parrots. Biol Lett 1:38-43.
McGraw KJ, Hill GE, Navara KJ, Parker RS. 2004. Differential accumula-
tion and pigmenting ability of dietary carotenoids in colorful finches.
Physiol Biochem Zool 77:484-491.
McGraw KJ, Safron RJ, Wakamatsu K. 2005. How feather colour reflects its
melanin content. Funct Ecol 19:816-21.
Mee A, Denny R, Fairclough K, Pullan DM, Boyd-Wallis W. 2005. Observa-
tions of parrots at a geophagy site in Bolivia. Biota Neotrop 5:321-324.
Meehan CL, Mench JA. 2002. Environmental enrichment affects the fear
and exploratory responses to novelty of young Amazon parrots. Appl
Anim Behav Sci 79:75-88.
Meehan C, Mench J. 2006. Captive parrot welfare. In: Manual of Parrot
Behaviour. Oxford: Blackwell Publishing. p 301-317.
Meehan C, Mench J. 2007. The challenge of challenge: Can problem solv-
ing opportunities enhance animal welfare? Appl Anim Behav Sci 102:
246-261.
Meehan CL, Garner JP, Mench JA. 2003a. Isosexual pair housing improves
the welfare of young Amazon parrots. Appl Anim Behav Sci 81:73-88.
Meehan CL, Millam JR, Mench JA. 2003b. Foraging opportunity and in-
creased physical complexity both prevent and reduce psychogenic feather
picking by young Amazon parrots. Appl Anim Behav Sci 80:71-85.
Meehan CL, Garner JP, Mench JA. 2004. Environmental enrichment and
development of cage stereotypy in Orange-winged Amazon parrots
(Amazona amazonica). Dev Psychobiol 44:209-218.
Mettke-Hofmann C, Winkler H, Leisler B. 2002. The significance of ecological
factors for exploration and neophobia in parrots. Ethology 108:249-272.
Moons CPH, Van Wiele P, Ödberg FO. 2004. To enrich or not to enrich:
Providing shelter does not complicate handling of laboratory mice.
JAALAS 43:18-21.
Moorhouse RJ. 1997. The diet of the North Island kaka (Nestor meriodona-
lis septentrionalis) on Kapiti Island. New Zeal J Ecol 21:141-152.
NRC [National Research Council]. 1996. Guide for the Care and Use of
Laboratory Animals. Washington: National Academy Press.
ILAR Journal
NRC. 2006. Guidelines for the Humane Transportation of Research Ani-
mals. Washington: National Academies Press.
Nuboer JF, Coemans MA, Vos JJ. 1992. Artificial lightening in poultry
houses: Do hens perceive the modulation of fluorescent lamps as flicker?
Br Poult Sci 33:123-133.
Ödberg FO. 1978. Abnormal behaviours (stereotypies). Proc First World
Congr Ethol Appl Zootechnics, Madrid. p 475-480.
Oviatt LA, Millam JR.1997. Breeding behavior of captive orange-winged
Amazon parrots. Exotic Bird Rep 9:6-7.
Paul E. 2005. A Guide to the Permits and Procedures for Importing Live
Birds into the US for Scientific Research and Display. Washington: Or-
nithological Council.
Pepperberg IM. 1995. Mirror use by African grey parrots (Psittacus erith-
acus). J Comp Psychol 109:182-195.
Pepperberg IM. 2006. Grey parrot cognition and communication. In:
Luescher AU, ed. Manual of Parrot Behaviour. Oxford: Blackwell
Publishing. p 133-145.
Pepperberg IM. 2007. Individual differences in grey parrots (Psittacus
erithacus): Effects of training. J Ornithol 148:S161-S168.
Prescott NB, Wathes CM, Jarvis JR. 2003. Light, vision and the welfare of
poultry. Anim Welf 12:269-288.
Prum RO, Torres R, Williamson S, Dyck J. 1999. Two-dimensional Fourier
analysis of the spongy medullary keratin of structurally coloured feather
barbs. Proc R Soc Lond B 266:13-22.
Reddy MB, Love M. 1999. The impact of food processing on the nutritional
quality of vitamins and minerals. In: Jackson LS, Knize MG, Morgan
JN, eds. Impact of Food Processing on Food Safety. New York: Kluwer
Academic/Plenum Publishers. p 99-106.
Romagnano A. 2006. Mate trauma. In: Luescher AU, ed. Manual of Parrot
Behaviour. Oxford: Blackwell Publishing. p 247-253.
Rowley I. 1997. Family cacatuidae (cockatoos). In: del Hoyo J, Elliott A,
Sargatal J, eds. Handbook of the Birds of the World, vol 4. Barcelona:
Lynx Editions. p 242-279.
Rozek JC, Danner LM, Stucky PA, Millam JR. 2010. Over-sized pellets
naturalize foraging time of captive orange-winged Amazon parrots
(Amazona amazonica). Appl Anim Behav Sci 125:80-87.
Russell WD. 1987. Common cage and aviary birds. In: Burr EW, ed. Com-
panion Bird Medicine. Ames: Iowa State University Press. p 2-7.
Russello MA, Avery ML, Wright TF. 2008. Genetic evidence links invasive
monk parakeet populations in the United States to international pet
trade. BMC Evol Biol 8:217.
Samour J. 2004. Toxicology. In: Samour J, ed. Avian Medicine. London:
Harcourt Publishers. p 180-192.
Scarl JC, Bradbury JW. 2009. Rapid vocal convergence in an Australian cock-
atoo, the galah Eolophus roseicapillus. Anim Behav 77:1019-1026.
Schachner A, Brady TF, Pepperberg IM, Hauser MD. 2009. Spontaneous
motor entrainment to music in multiple vocal mimicking species. Curr
Biol 19:831-836.
Schmidt MF. 2010. An IACUC perspective on songbirds and their use in
neurobiological research. ILAR J 51:424-430.
Schulte MS, Rupley AE. 2004. Avian care and husbandry. Vet Clin Exot
Anim 7:315-350.
Scott P. 1995. Zoonotic, legal and ethical aspects. In: Harcourt-Brown N,
Chitty J, eds. BSAVA Manual of Psittacine Birds, 2nd ed. Gloucester:
British Small Animal Veterinary Association. p 280-287.
Seibert LM. 2006. Social behaviour of psittacine birds. In: Luescher AU, ed.
Manual of Parrot Behaviour. Oxford: Blackwell Publishing. p 43-47.
Shepherdson DJ, Mellen JD, Hutchins M, eds. 1998. Second nature: Envi-
ronmental enrichment for captive animals. Washington: Smithsonian
Institution Press.
Volume 51, Number 4 2010
Shuck-Paim C, Borsari C. 2009. Means to an end: Neotropical parrots
manage to pull strings to meet their goals. Anim Cogn 12:287-
301.
Sibley CG, Ahlquist JE. 1990. Phylogeny and Classification of Birds: A
Study in Molecular Evolution. New Haven: Yale University Press.
Silva T. 1991. Psittaculture: The Breeding, Rearing and Management of
Parrots. Surrey: Birdworld.
Snyder NFR, Wiley JW, Kepler CB. 1987. The parrots of Luquillo: Natural
history and conservation of the Puerto Rican parrot. Los Angeles: West-
ern Foundation of Vertebrate Zoology.
Snyder NFR, Koenig SE, Koschmann J, Snyder HA, Johnson TB. 1994.
Thick-billed parrot releases in Arizona. Condor 96:845-862.
Stanford M. 2006. Effects of UVB radiation on calcium metabolism in psit-
Downloaded from https://academic.oup.com/ilarjournal/article-abstract/51/4/409/676068 by guest on 17 November 2019
tacine birds. Vet Rec 159:236-241.
Stoodley AAJ, Hadgkiss IM, Rance LA. 1992. Feeding, housing and breed-
ing. In: Price CJ, ed. Manual of Parrots, Budgerigars, and Other Psittacine
Birds. Gloucestershire: British Small Animal Veterinary Association.
p 189-202.
Stradi R, Pini E, Celentano G. 2001. The chemical structure of pigments in
Ara macao plumage. Comp Biochem Physiol B 130:57-63.
Tokita M, Kiyoshi T, Armstrong KN. 2007. Evolution of craniofacial nov-
elty in parrots through developmental modularity and heterochrony.
Evol Dev 9:590-601.
Turner GV. 1987. Zoonotic diseases. In: Burr EW, ed. Companion Bird
Medicine. Ames: Iowa State University Press. p 221-225.
Turner WT. 1992. Handling and clinical examination. In: Price CJ, ed. Man-
ual of Parrots, Budgerigars, and Other Psittacine Birds. Gloucestershire:
BSAVA. p 7-15.
UFAW [Universities Federation for Animal Welfare]. 2010. Handbook
on the Care and Management of Laboratory and Other Research
Animals, 8th ed. Hubrecht R, Kirkwood J, eds. Oxford: Wiley-
Blackwell.
Ullrey DE, Allen MA, Baer DJ. 1991. Formulated diets versus seed mix-
tures for psittacines. J Nutr 121:S193-S265.
van Zeeland YRA, Spruit BM, Rodenburg TB, Riedstra B, van Hierden YM,
Buitenhuis B, Korte SM, Lumeij JT. 2009. Feather damaging behaviour
in parrots: A review with consideration of comparative aspects. Appl
Anim Behav Sci 12:75-95.
Webb NV, Famula TR, Millam JR. 2010. The effect of rope color, size and
fray on environmental enrichment device interaction in male and female
orange-winged Amazon parrots (Amazona amazonica). Appl Anim Be-
hav Sci 124:149-156.
Welle KR, Luescher AU. 2006. Aggressive behavior in pet birds. In:
Luescher AU, ed. Manual of Parrot Behaviour. Oxford: Blackwell
Publishing. p 211-218.
Werdenich D, Huber L. 2006. A case of quick problem solving in birds:
String pulling in keas, Nestor notabilis. Anim Behav 71:855-863.
Wilson L. 2005. Biting and screaming behavior in parrots. In: Rupley AE,
ed. Veterinary Clinics of North America, Exotic Animal Practice: Avian
Pet Medicine. Philadelphia: WB Saunders. p 173-179.
Wilson GH. 2006. Behavior of captive psittacids in the breeding aviary. In:
Luescher AU, ed. Manual of Parrot Behaviour. Oxford: Blackwell Pub-
lishing. p 281-289.
Wilson L. 2007. Psittacine behaviour in the examination room: Practical
applications, handling, and restraint. J Exot Pet Med 16:24-29.
Wolf P, Bayer G, Wendler C, Kamhues J. 1998. Mineral deficiencies in pet
birds. J Anim Physiol An N 80:140-146.
Wolf P, Graubohm S, Kamphues J. 2002. Experimental data on feeding ex-
truded diets in parrots. In: Proc Joint Nutrit Symp, Antwerp, August
21-25. p 137.
423