The welfare and suitability of parrots as companion animals: a review

263

copy 2006 Universities Federation for Animal WelfareThe Old School Brewhouse Hill WheathampsteadHertfordshire AL4 8AN UK

Animal Welfare 2006 15 263-276ISSN 0962-7286

The welfare and suitability of parrots as companion animals a review

M Engebretson

Animal Protection Institute 1122 S Street Sacramento CA 95814 USA email monicaapi4animalsorg

Abstract

In recent years there has been an increased interest in studies related to the welfare of avian species commonly kept as companionanimals specifically those in the order Psittaciformes commonly referred to as lsquoparrotsrsquo During this time the biology and behaviourof wild parrots has also become better understood aiding the assessment of welfare in captive environments The impact of the pettrade on wild parrot populations has also become clear This order now has more globally threatened species than almost any othermajor group of birds Many significant aspects of parrot behaviour in the wild such as flocking social interaction with conspecificsforaging on a variety of foods and flight are denied to varying degrees to parrots kept as companion animals Captive parrots showhigh levels of stereotypy suggesting poor welfare Welfare may be improved by appropriate environmental enrichment and changesin the social environment of captive parrots kept as companion animals however such changes require that caretakers have suffi-cient knowledge resources and motivation to accommodate such conditions The concept of companion animal suitability is animportant consideration when developing regulations or policy aimed at improving the welfare of animals kept as companionsAlthough individual exceptions exist and the level of suitability may vary depending on species in general their presence in the pettrade has resulted in serious animal welfare and conservation challenges for parrots indicating that these animals may be unsuitableas human companions

Keywords animal welfare captive parrots captive wildlife companion animals pet ownership pet trade

IntroductionAlthough an accurate estimate of the total number of petbirds in the US is impossible to determine because thenumbers vary wildly from source to source it is generallyaccepted that birds (including parrots finches and canaries)are the fourth most popular companion animal after fishcats and dogs respectively (Kid amp Kid 1998 Meyers 1998)Unlike cats and dogs birds are not typically considereddomesticated animals even when bred in captivity This isdue in part to the fact that many bird species produced forthe pet trade are only one or two generations removed fromthe wild and as such retain most if not all of their wildinstincts and behaviours (Davis 1998 Graham 1998) Inaddition many bird species that are bred and traded ascompanion animals also remain physically indistinguish-able from their wild counterparts with the few exceptionsof those birds which have been hybridised or selectivelybred to express colour mutationsParrots are a well-defined group of birds that are so distinc-tive (small to medium sized with stout hooked bills and amoveable upper mandible) that their affinities to other birdtaxonomies remain unclear (Gill 1990) Species within theparrot family range in size from the relatively smallbudgerigars cockatiels and lovebirds and medium-sized

conures amazons and African greys to large-sizedcockatoos and macaws Due in part to their popularity aspets the parrot family also contains a greater proportion ofthreatened and endangered species than any other largefamily of birds (Gill 1990)Some people believe that it is wrong to keep parrots as petsout of concern that birds suffer from being deprived of theirfreedom and ability to express natural behaviour such asflight (Kid amp Kid 1998) whereas others disagree citing thehuman benefits of bird companionship (Voren 1995 Kid ampKid 1998) and protection from environmental hazards asjustification for keeping parrots as pets (Desborough 1994)Some are concerned that the pet trade threatens the speciesin the wild or that escaped pet parrots could pose a threat tonative birds either through disease transmission or resourcecompetition (Jackson 2003) However some believe thatthe captive breeding and private possession of parrots forpet purposes serve to conserve wild species (Desborough1996 Kid amp Kid 1998) All parties in the debate arrive atdifferent opinions on the same issue by evaluating varioussets of criteria placing different degrees of importance oneach criterion and perhaps having varying levels ofknowledge about relevant animal welfare and conservationissues

Universities Federation for Animal Welfare Science in the Service of Animal Welfare

264 Engebretson

Review approachSchuppli and Fraser (2000) developed a systematic analysisto evaluate the suitability of different species as companionanimals based on a wide range of issues such as thosedescribed above that are relevant to such an assessmentTheir analysis considered three main criteria the welfare ofthe animal the welfare of others (including humans andother animals) and the welfare of the environment Thispaper will review the current literature on the welfare ofcaptive birds and utilise the framework described bySchuppli and Fraser (2000) to assess the suitability ofparrots as companion animals

Welfare of the animalThe examination of animal welfare is a useful tool in deter-mining the suitability of keeping a particular species as acompanion animal This is because welfare describes thestate of an animal at a specific time and can be lsquogoodrsquo orlsquopoorrsquo regardless of what people think about the morality ofusing such animals in a particular wayThe lsquofive freedomsrsquo of the Farm Animal Welfare Council(1992) have been used to evaluate animal welfare for manyspecies and are used as part of the Schuppli and Fraser(2000) criteria for determining companion animal suit-ability These freedoms are (1) freedom from hunger thirstand malnutrition (2) freedom from disease and injury(3) freedom from physical and thermal discomfort(4) freedom from fear distress and other negative psycho-logical states and (5) freedom to carry out most normalforms of behaviour Although many of these freedoms areinter-related mdash for example deprivation of the freedom toexpress normal forms of behaviour may cause a negativepsychological state that results in physical injury mdash I willattempt to evaluate each freedom individually with theexception of the last two freedoms (4 and 5) which will bediscussed together

Freedom from hunger thirst and malnutritionThis first freedom is further defined as the animal havingldquoready access to fresh water and a diet to maintain fullhealth and vigourrdquo (Farm Animal Welfare Council 1992)Common captive parrot caging environments provide ampleaccess to both food and water so it would appear that inmost cases the first freedom is met However as Schuppliand Fraser (2000) have pointed out the nutritional require-ments of the species must be adequately known and suitablefoods must be available to the owner in order to assure ldquofullhealth and vigourrdquoIt has been estimated that malnutrition is responsible for upto 90 of all clinical conditions seen by avian practitioners(Harrison 1998) It is well recognised among avian profes-sionals that seed diets lack nutrients and are high in fathowever seed diets remain the most widely available andmost commonly fed pet bird diet (Harrison 1998 Reid ampPerlberg 1998)Although a number of high-quality formulated diets areavailable in the form of pellets dietary standards are rela-

tively non-existent and it is unlikely that detailed nutritionalrequirements will ever be documented for all the variousspecies of birds kept as pets (Harrison 1998 Reid ampPerlberg 1998) Despite this many labels give the impres-sion that the diet is complete when in fact the food containsonly minimum requirements which may not provide suffi-cient nutrition for some birds Further complicating mattersmany avian professionals recommend that birds not be feda pellet-only diet and that formulated pellet diets be supple-mented with fresh fruit and vegetables to ensure optimalnutrition and health (Reid amp Perlberg 1998) Many nutri-tional problems diagnosed in birds seem to arise fromconfusion on the part of the caretaker over conflicting infor-mation for achieving balanced nutrition (Donoghue 1997)

Freedom from disease and injuryThe existence of adequate veterinary knowledge and avail-ability is necessary for the fulfilment of this freedomDuring the past 20 years research by avian practitioners andacademics and the skills of avian veterinarians haveimproved considerably Speciality avian practices havetailored diagnostic tests emergency medical procedures andanaesthesia monitoring for birds (Altman 1998 Flammer1998) However despite the advances in avian veterinarymedicine and the availability of veterinarians specialising inavian care and treatment only 117 of bird-owning house-holds currently seek veterinary advice for their birds(American Veterinary Medical Association 2002)There are a number of viral bacterial fungal and parasiticdiseases that pet birds can become infected with but viralinfection is one of the major causes of mortality in parrots(Ritchie et al 2000) The four most common viral infectionsinfecting pet parrots are avian polyomavirus proventriculardilatation disease (PDD) psittacine beak and featherdisease (PBFD) and Pachecorsquos disease (Ritchie et al 2000)There is no cure for avian polyomavirus although there is areliable vaccine on the market and there is no known cureor vaccine for PBFD or PDD Although a vaccine forPachecorsquos disease (PsittimuneTM Biomune Company 8906Rosehill Road Lenexa KS 66215 USA) was registered bythe United States Department for Agriculture for use in petbirds in 1990 (Center for Veterinary Biologics 2005) it isnot routinely used except in the face of an outbreak(Romagnano 2003a) Some veterinarians have had successin treating birds in early stages of the disease withAcyclovir an anti-herpesvirus agent (Ritchie 1997)Avian chlamydiosis caused by Chlamydophila psittacicommonly known as psittacosis or lsquoparrot feverrsquo is one ofthe more common bacterial infections in birds and is trans-mittable to humans (see Welfare of others below) Birdswith mild infection may be asymptomatic carriers and mayshed the disease for many months or years with no outwardsign of illness The organism is shed in the faeces and nasaldischarge of infected birds is resistant to drying and canremain infectious for several months (Centers for DiseaseControl and Prevention [CDC] 1998) Severely ill birdsexhibit clinical signs of diarrhoea severe lethargy weightloss poor feather condition conjunctivitis nasal discharge

copy 2006 Universities Federation for Animal Welfare

A review of parrots as companion animals 265

and anorexia (CDC 1998) There is no vaccine for Cpsittaci and it can be very difficult to diagnose and screenfor because infected birds may test negative for the disease(CDC 1998) In birds the condition is often fatal but veteri-narians have had success in treating infected birds withantibioticsAspergillosis caused by the fungus Aspergillus is the mostcommon fungal infection in captive birds and can be acuteor chronic The fungus is commonly found in nearly allenvironments but typically only causes disease or illness inbirds whose immune system has already been compromisedby stress malnutrition poor husbandry (ie inadequate venti-lation mouldy food etc) or previous injury to the respira-tory system (Eifert et al 2003)Birds with acute aspergillosis have severe difficulty inbreathing loss of or decreased appetite frequent drinkingand urination and even sudden death (Kearns 2003) Thechronic form is more common and is difficult to diagnoseAs a result the bird may not become symptomatic until thedisease is beyond cure Once diagnosed aspergillosis canbe treated with antifungal drugs and surgery may beperformed to remove lesions but the prognosis is oftenmixed (Kearns 2003)

Freedom from physical and thermal discomfortThese criteria essentially require that the animal is providedwith an environment that protects him or her from physicalinjury or weather extremes that could lead to considerablediscomfort or illness In order for this freedom to be met thephysical and environmental needs of the animal must beknown and the caretaker must be capable of providing thoseneeds (Schuppli amp Fraser 2000)Like mammals birds are warm-blooded and as such arecapable of regulating their own body temperature within areasonable range The feathers serve a function similar tothat served by fur on many mammal species Although it isadvised that caretakers avoid extreme temperature changesand draughts (McCluggage amp Higdon 1999) the require-ments for accommodating the thermal needs of birds arerelatively simple and not dissimilar from the requirementsfor keeping cats dogs or small mammals such as guineapigs or hamstersIn the US pet parrots are typically housed in cagesConfinement to the cage protects the bird from incurringphysical injury from predators including household dogsand cats or from other household hazards such as flyinginto windows or chewing electrical cords Even if asdiscussed above the diet provided is a nutritionally inade-quate all-seed diet if provided in ample quantity and withample water captive birds are generally free from thephysical discomfort of hunger and thirst At first glance itappears that captive birds experience less discomforts thantheir wild counterparts which must dodge predators endureinclement weather and search daily for food and waterHowever Graham (1998) reported that despite theseemingly care-free life of a caged bird necropsies of petbirds often reveal evidence of ldquoa life beset with stressrdquo in

the form of stress-related lesions in birds submitted forpost mortem examinationGraham (1998) postulated that the stress seen in captivebirds may be due in part to physical and behavioural restric-tions imposed by standard captive environments He wroteldquoIt would seem that the ideal enclosure for a captive bird isone of such size and equipped with such internal furnishingsthat the bird would have no awareness of its captivityAnything less is a compromise and acceptance on the partof the keeper that the kept may or will be subject to thestresses imposed by a lesser or greater degree of restrictionof its normal behavioursrdquoGrahamrsquos recommendations for an optimal captive environ-ment seem to exceed the means of the average privateowner Although cage sizes do vary a cage is typicallyconsidered adequate if the birdrsquos extended wing-span andlength of tail can be freely accommodated within the cage(Graham 1998) As birds do survive and even reproduce insuch enclosures it is generally accepted as adequate housingfor pet birds However survival and successful breedingalone do not indicate whether welfare is good as manyanimals are successfully bred under captive conditions thatare found to have severe welfare problems (Fraser amp Broom1990)

Freedom from fear distress and other negative psychological states and freedom to carry out most normal forms of behaviourIn order to meet the fourth freedom lsquoFreedom from feardistress and other negative psychological statesrsquo animalsmust be housed and treated in a manner that avoids mentalsuffering The determination of mental suffering in animalsis difficult however some mental distresses are manifestedphysically such as the stress lesions described by Graham(1998) self mutilation or other outward displays ofabnormal or stereotypic behaviourThe distinction between normal and abnormal behaviour iscomplicated because some behaviour designated aslsquoabnormalrsquo in captive animals is actually derived fromnormal behaviour that fails to serve a practical function in acaptive situation The freedom to express normal behaviourand freedom from distress appear to be inextricably linkedin captive parrots and other birds kept as pets (Sargent ampKeiper 1967 Keiper 1969 King 1993 Graham 1998 vanHoek amp ten Cate 1998 King 2000 Garner et al 2003bMeehan et al 2003a 2004 Meehan et al 2003b) For thisreason I will consider the last two freedoms concomitantlyIf an individual animal is having difficulty in coping with itsenvironment or is failing to cope then its welfare is poorbut if strongly preferred resources and opportunities forbehaviour are available and normal behaviour can beshown then good welfare is indicated (Broom 1996) Theevaluation of welfare should attempt to encompass thepsychological aspects of subjective feelings (Broom 1996Duncan 1996) Although parrot caretakers frequentlydescribe their parrots as feeling lsquohappyrsquo lsquosadrsquo orlsquodepressedrsquo these emotional states are difficult to measure

Animal Welfare 2006 15 263-276

266 Engebretson

empirically and as such this discussion will focus on thephysically expressed behaviours that are indicative ofwelfare statesParrots are exceptionally social birds In the wild parrotstypically travel in large flocks flying miles each day insearch of a wide variety of food and may congregate into anightly roost of hundreds or even thousands of socialconspecifics (Gilardi amp Munn 1998) Stamps et al (1990)postulated that the formation and maintenance of socialrelationships within a flock may be as critical for survival aspredator avoidance and foraging efficiency and Birchall(1990) reported that wild parrots may use 90 of their timeforaging for food and preening their partnersSchuppli and Fraser (2000) explained that ethical objectionsto keeping a companion animal arise if benefits to the ownerare achieved to the detriment of the animal They contendedthat ldquokeeping a particular species might lead to suffering ifthe animals are prevented from carrying out an importantelement of their natural behaviourrdquo Birds are routinelydenied two of their most fundamental natural behavioursflying and socialisation It has been suggested that thedenial of these activities can cause both physical (Graham1998) and behavioural abnormalities in captive parrots (vanHoek amp ten Cate 1998 Garner et al 2003b Meehan et al2003a 2004 Meehan et al 2003b) Parrots kept as pets areoften housed alone or in pairs in small cages incapable ofaccommodating flight (van Hoek amp ten Cate 1998) Evenwhen not confined to cages pet parrots are commonly phys-ically disabled through one of several deflighting proce-dures to restrict or prevent flight (Hesterman et al 2001)There are several methods of deflighting includinglsquopinioningrsquo the surgical removal of the distal wing portionand lsquotenonectomyrsquo the surgical cutting and cauterisation ofthe main wing tendon preventing extension of the wing(Hesterman et al 2001) The most common form ofdeflighting in captive birds kept as pets is lsquowing clippingrsquowhich is a relatively simple technique that typicallyinvolves the non-surgical unilateral cutting of the primary(flight) feathers This deflighting procedure is temporaryand birds regain their flying ability following the naturalmoult and re-growth of feathers within a year to 18 monthsHesterman et al (2001) examined the welfare implicationsof various deflighting procedures on captive birds andpointed out that although deflighting limits or denies thebird the ability to express the normal behaviour of flight itcan allow them to express other behaviours (climbingexploring socialisation with human caretakers) that wouldotherwise be suppressed if confined to a cageHowever deflighting does not guarantee better welfareFlight provides cardiovascular exercise beneficial to healthand allows birds to escape swiftly from predators includinghousehold cats and dogs and prevents birds from incurringinjury when falling from high perches wing clipping mayalso initiate feather-plucking behaviour in some parrots(Forbes amp Glendell 1999 Hesterman et al 2001) Somebehaviourists and veterinarians are now recommendingagainst wing clipping for the physical and psychological

well-being of the bird and encourage the use of basicobedience training to assist in the control of flighted birds(Forbes amp Glendell 1999 McCluggage amp Higdon 1999)Whether or not wing clipping benefits a birdrsquos overallwelfare in captivity may be irrelevant to the question ofwhether the birds make suitable pets Perhaps a morerelevant question is whether it is acceptable to keep a partic-ular animal in captivity as a companion animal if ensuringhis or her safety or compatibility in the home requires thathe or she be physically disabledCompanion dogs and cats undergo routine physical alter-ations such as spaying or neutering declawing for cats andtail docking and ear cropping in dogs Although the latterthree procedures are controversial spaying and neuteringare generally viewed as beneficial and acceptable physicalalterations and none of these procedures interrupts theanimalsrsquo natural primary mode of locomotionAlthough spaying or neutering is a physical alteration thateffectively disables an animalrsquos reproductive ability theprocess of spaying or neutering also reduces and in somecases eliminates reproductive behaviour due to changes inhormonal activity that accompany the physical removal ofthe reproductive organs leading to an assumption that thelsquodesirersquo to engage in such behaviour is reduced or elimi-nated The welfare of the progeny of the reproductivelyintact animal can also be weighed against any potentialwelfare benefits of allowing reproductive behaviour incompanion animalsIt is unknown whether deflighting a bird reduces or elimi-nates his or her natural instinct or lsquodesirersquo to fly Howeverdeflighted birds who regain their physical ability to flyusually attempt flight suggesting that deflighting alters thebirdrsquos ability to fly but not necessarily his or her interest indoing so

Abnormal behaviour and stereotypies in captive parrotsKnowledge of the biological functioning of parrots and thesystems used by them to cope with adversity can be usefulin the selection and interpretation of welfare indicators Theextent to which animals are positively or negatively affectedby their captive environments is likely to also depend ontheir cognitive abilities (Held et al 2001) Parrots have beenshown to have high-level cognitive abilities (Pepperberg1999 2004) and have been likened to primates and humantoddlers in terms of their intelligence and psychological andsocial needs (Birchall 1990 Davis 1998) These capabilitiesmay be an important factor in the apparent high suscepti-bility of parrots to developing abnormal behaviour incaptivity (Birchall 1990)Stereotypies are abnormal repetitive unvarying and func-tionless behaviours that are often performed by captive anddomesticated animals housed in barren or restricted envi-ronments and are mostly absent in the wild and are rela-tively infrequent in large environmentally enrichedenclosures (Field amp Thomas 2000 Garner et al 2003a)Stereotypic behaviour is often considered an indicator of



poor welfare (Mason 1991 Broom 1996) With theexception of poultry there have been few systematic scien-tific studies of stereotypic behaviour in captive birds kept aspets (van Hoek amp ten Cate 1998 Seibert et al 2004)Three studies of stereotypic behaviour in laboratory cagedPasseriformes commonly known as lsquosongbirdsrsquo describedtwo common repetitive stereotypies in caged birds spotpicking and route tracing in caged canaries (Serinuscanarius [Sargent amp Keiper 1967 Keiper 1969] and routetracing in blue and marsh tits (Parus caeruleus and Ppaulstris [Garner et al 2003a])In spot picking a bird will repeatedly touch the tip or side ofthe bill to a particular spot mdash either an object or a body partIn route tracing a bird will follow a precise and invariableroute within its cage This behaviour is similar to thelsquopacingrsquo often seen in caged mammals (Sargent amp Keiper1967) Stereotypy levels were significantly reduced incanaries which were provided with opportunity for socialinteraction with other canaries but interaction with anotherspecies had no effect (Sargent amp Keiper 1967) suggestingthat deprivation of social interaction with the same speciescan contribute to or cause poor welfare Keiper (1969)revealed an association between spot picking and captivefeeding conditions suggesting that the behaviour is frus-trated natural foraging behaviour Canaries which wereforced to work for food compared to those who had freeaccess to food also showed a reduction in spot-pickingbehaviour Route tracing was linked to the size of theenclosure with a significant reduction in the behaviourachieved when birds were housed in an aviary Interestinglythe housing of birds in flight cages which were more thantwice the size of standard cages did not significantly reduceroute-tracing behaviour (Keiper 1969)The recent studies of Meehan et al (2003a 2004 and 2003b)and Garner et al (2003b) have examined the causes ofstereotypies specifically in captive parrots Garner et al(2003b) found that stereotypy in captive orange-wingAmazon parrots (Amazona amazonica) was correlated withpoor performance on the same psychiatric task (thelsquogambling taskrsquo) as stereotypy in autistic and schizophrenichuman patients suggesting ldquopotential psychological distressin animals showing these behavioursrdquo Similarly Bordnicket al (1994) compared feather-picking behaviour in parrotsto compulsive and impulsive human disorders such astrichotillomania mdash an impulse control disorder in humanscharacterised by the removal of hair resulting in noticeablebald patches Feather plucking has also been compared tothe commonly reported obsessive-compulsive hand-washing behaviour in humans (Seibert et al 2004)Meehan et al (2003a 2004) showed that environmentalenrichment appropriate foraging substrates and increasedphysical complexity significantly reduced the developmentand performance of oral (feather-picking) andor locomotorstereotypies in parrots Meehan et al (2003a) found thatbirds caged in isosexual pair housing positively affected thewelfare of captive parrots by eliminating the developmentof stereotypy without jeopardizing the ability of parrots to

relate positively with humans This finding stands incontrast to lsquopopularrsquo literature on parrot care which recom-mends that pet parrots not be pair housed under the assump-tion that the birds will form emotional bonds to each otherrather than to the human caretaker thereby making themless desirable as pets (Blanchard 1999)It is also important to note that in the research design ofMeehan et al (2003b) and Meehan et al (2004) singlyhoused birds were caged directly across from one anotherand were housed within the same building structure as suchthe singly housed parrots had visual contact with at leastone other parrot of the same species and had vocal contactwith several others (Meehan et al 2003b Meehan et al2004) This is in contrast to the condition in which manycaptive parrots are kept mdash without any visual or vocalcontact with members of their own species Thus furtherstudies would be required to determine the impact of totalisolation from social conspecifics on the development ofstereotypy in caged parrots to accurately reflect conditionsunder which pet parrots are typically housedThe combined results of the studies on stereotypicbehaviour in captive birds (both songbirds and parrots)suggest that the development of locomotor stereotypy (egroute tracing pacing) is related to lack of space and physicalcomplexity and that oral stereotypy (eg feather picking barchewing) is related to lack of opportunity to performforaging behaviour Lack of social interaction with the samespecies appears to contribute to the development of bothoral and locomotor stereotypy (Sargent amp Keiper 1967Keiper 1969 Meehan et al 2003a 2004 Meehan et al2003b)Although the studies also suggest that changes in thecaptive environment (cage size enrichment socialisation)can improve the welfare of captive parrots such changesrequire that the owner has sufficient knowledge resourcesand motivation to fulfil these requisites and that the motiva-tion to provide such complex care regimes is sustainedthroughout the life of the animal Schuppli and Fraser(2000) explained that ldquoAnimal welfare may also be jeopar-dised if the owner loses interest in or commitment to theanimalrdquo and that ldquoconsistent care may also be jeopardised ifanimals are very long lived For example parrots in captivitycan live 30ndash80 years (Forshaw 1973) as do many primatessuch pets may outlive their owners or the owners may losethe interest or ability to provide care with the result that theanimal is put into a shelter or is passed through a series ofownersrdquo Field and Thomas (2000) noted that even in zoosituations where caretakers are paid to provide care forparrots and enrichment is well recognised as an integral partof captive bird husbandry enrichment is the first task to bedismissed when time andor staff shortages occurIf consistent and high-quality care cannot be guaranteed ina professional zoological setting it is difficult to imaginehow consistent high-quality care can be reasonablyexpected from the general public Indeed evidence suggeststhat many parrots kept as companion animals are notreceiving optimal care In 1998 the World Parrot Trust


268 Engebretson

stated that perhaps as many as 50 of all companion parrotswere kept in cramped and inadequate conditions Thisstatistic supports the assertion of Davis (1998) thatldquoalthough birds are intelligent and highly responsive to andaware of their surroundings their treatment seldom reflectsthis factrdquoProper care can be enforced legally if federal or state lawsare written in such a way as to specifically describestandards of care and to require that those standards be metin order to possess a certain animal Standards of care forcaptive birds are almost non-existent and if they do existoften require only minimum care such as requiring that thecage be wide enough in at least one direction to accommo-date completely stretched wings (Animal ProtectionInstitute 2005) Therefore providing the care needed toavoid the development of stereotypic behaviour in captivebirds is entirely voluntary on behalf of the possessor whomay not even be aware of the need

RelinquishmentLack of interest in or commitment to providing specialisedcare for a long-lived species may also contribute to pet birdsbeing acquired and resold given away or abandoned atsome time in their lives There are currently more than 100self-described bird rescue facilities in the US and severalshelters especially in metropolitan areas have reported anincrease in the number of relinquished birds in recent yearsIn addition sightings of free-flying parrots and establishedflocks suggest that in addition to accidental escapes somepet birds may be intentionally set free when their caretakerstire of them The number of birds released each year andexact estimates of naturalised parrot populations areunknown (Mabb 2002)Clubb (1998) explained that ldquomany birds are given upwithin a few years of being brought into their ownerrsquoshomesrdquo and noted that ldquoin many cases owners simply donot have accurate expectations when they purchase parrotsor have not been properly educated and made aware ofnormal psittacine behaviourrdquo Kid and Kid (1998) reportedthat ldquoNoisiness is the second (after messiness) mostcommon complaint of parrot ownersrdquo and Meehan et al(2003b) noted that ldquoincessant screaming is one of theprecipitating factors for parrot neglect and abuserdquo

Procurement and transportationThe final question in evaluating the welfare of the animalunder the Schuppli and Fraser (2000) check list ofcompanion animal suitability is whether or not there is anyappreciable risk of suffering injury illness or death arisingfrom procurement andor transportation of a species for thepet trade Pet parrots may be wild-caught or captive bredEach of these procurement methods has different welfareimplications and therefore will be discussed separately

Wild-captureAlthough the 1992 US Wild Bird Conservation Act(WBCA) prohibited imports of wild parrots and reduced theUS from the largest importer of birds to one of the smallest

an unknown number of wild-caught birds are illegallyimported over the USndashMexico border each year (Michels2002) Parrots are also legally and illegally traded withintheir countries of origin and are legally imported orsmuggled into the European Union and throughout AsiaThe high mortality rates inconsistent and insufficient lawsand millions of birds of different species involved in thetrade mean that it is impossible to determine the exactnumber of wild-caught birds traded (Knights amp Currey1990)Adult or juvenile parrots may be captured by large netssprung when parrot flocks congregate on the ground near awater or food source (May amp Hovetter 2002) or may besnared in trees with fishing line traps (Riupassa personalcommunication 2001) whereas others may be netted at nestcavity entrances (Bucher et al 1992) Neonatal birds aretaken directly from nests either by scaling the trees andreaching into the nest cavity or by felling the tree andcutting into the nest cavity to remove the young birds(Bucher et al 1992)There are substantial risks inherent in any live capture ofwild animals Physical deterioration as a result of stress orcapture myopathy mdash a syndrome characterised by severeand often fatal degeneration of skeletal muscle mdash has beenobserved in a wide variety of mammalian and avian speciesassociated with capture and handling (Wobeser 1994) Birdsare especially fragile Climatic changes and stress duringtransport can cause significant mortality even whenimported legally (Knights amp Currey 1990) Nicaraguanresearchers estimate that in order to compensate for mortal-ities up to four times as many parrots are captured thanmake it to market (Michels 2002) Wright et al (2001) foundthat mortality rates from poaching were significantly greaterthan mortality due to natural causes

Domestic productionAfter the passage of the WBCA dramatically reduced thesupply of wild-caught birds for the pet trade in the USattention focused on domestic production The appearanceof hand-raised baby parrots in the pet market increased thepopularity of keeping parrots as pets (Wilson 1998) in partbecause the neonatal and juvenile stage is a time when thelsquopet qualityrsquo of captive parrots is considered the highest(Clubb 1998)To meet the demand for pet birds many species of parrotsespecially budgerigars cockatiels lovebirds and smallconures are mass-produced for the pet trade (Vriends 1996Low 2000 Blanchard 2001) As illustrated in Vriends(1996) and described in the experimental design in Millamet al (1995) modern breeding facilities typically houseparrots indoors in individual paired breeding cagesfurnished with one or two perches food and water recepta-cles and a nesting box Despite the design similarities tolsquopuppy millsrsquo bird production facilities or lsquobird millsrsquo havenot been met with the same scrutiny from the animalwelfare community and the general public This may be dueto the familiarity of seeing birds confined to cages althoughthere is no empirical evidence that suggests that the welfare



of caged breeding dogs is lower than the welfare of cagedbreeding parrotsSome parrots produced for the pet trade are bred in free-flight colony aviary situations that allow opportunity forfree mate selection social interaction and physical activityincluding flight Although this situation has obvious welfareadvantages it offers less control over the breeding processless access to young for hand-raising purposes and may becost and space prohibitive for some breedersThere currently exist no legal standards governing birdproduction facilities whether bred commercially or forresearch purposes The US Animal Welfare Act (AWA) mdashlegislation passed in 1966 mdash extends protection to certain

warm-blooded animals maintained by certain animaldealers transporters exhibitors and research facilitiesBirds were excluded from the AWA until 2000 but standardsfor regulating breeding facilities are still in developmentand birds housed and used for research purposes will not becovered Ironically the very parrots used at universities tostudy parrot welfare will not be covered by the AWAAccording to unpublished data cited in Meehan et al (2004)96 of the orange-wing Amazon parrots in the researchresource colony at the University of California at Davisperform locomotor andor oral stereotypiesIn order to produce hand-raised parrots chicks are typicallyremoved from parents shortly after hatching (in some caseseggs are removed from the nest and hatched in anincubator) Unweaned chicks are fed a liquefied or semi-liquefied diet by oral gavage and maintained in thermallycontrolled brooders until they have sufficient feathers tomaintain their own body temperature (Vriends 1996)Although lsquopopular literaturersquo suggests that hand-raisedparrots make superior pets to parent-reared parrots(Blanchard1999) hand-rearing has the potential to producephysical as well as behavioural problems in parrots(Harcourt-Brown 2004) There are many risks involved inthe hand-feeding of young parrot chicks especially if thefeeder is inexperienced in hand-feeding techniques (Harris1997) Problems associated with improper hand-feedinginclude aspiration pneumonia which results from foodinhaled into the lungs of the bird burned or puncturedcrops which result from forceful feeding or feeding formulathat is too hot and malnutrition and starvation which resultfrom feeding food of inadequate nutritional value or inade-quate amounts (Romagnano 2003b) As there is no formalveterinary reporting system to track the incidence of hand-feeding injuries and as some injuries may go untreated bythe owner it is impossible to determine the frequency ofsuch injuriesA recent study by Harcourt-Brown (2003) found that 44of hand-reared African grey parrots (Psittacus e erithacus)suffered from a condition known as osteodystrophy definedas a failure of the normal development of bone The clinicalsigns of this condition are distortion and enlargement of thebones susceptibility to fracture and abnormal posture andgait (Blood amp Studdert 1988) Further studies by Harcourt-Brown (2004) suggested that premature physical activity in

hand-reared chicks my exacerbate the effects of a deficientdiet and contribute to skeletal deformity Parent-rearedchicks are naturally confined to the nest and receive skeletalsupport from huddling with siblings (Harcourt-Brown2004) Hand-fed birds are typically removed from the nestduring feeding and allowed to run around during and afterthe feeding thus incurring more physical exercise and morestress on their growing bones Limiting movement untilbone growth is complete may reduce the incidence of bonedeformities in hand-raised parrot chicks (Harcourt-Brown2004)It has also been suggested in recent years that hand-rearingcan influence the later development of aberrant behaviourssuch as stereotypy feather plucking and phobic behaviour(Lightfoot 2002) Studies suggest that in animals withhighly dependant young parental care influences behaviourdevelopment after nutritional independence and results inbetter welfare (Nimon amp Broom 1999) Recent researchalso suggests that parent-reared chicks that are handledregularly by humans exhibit tameness without the psycho-logical or physical risks of hand-rearing (Aengus amp Millam1999 Collette et al 2000) Aengus and Millam (1999) notedthat although continued handling of parent-reared chickswould probably be necessary to maintain tamenessldquoneonatal handling of parent-raised parrots provides a lowlabor and low technology alternative to artificial rearing asa means of initially taming birds thereby improving theiradaptation to life in captivityrdquoThe potential for physical injury in hand-fed birds can bereduced if human caretakers are adequately trained andskilled in hand-feeding techniques In recognition of thisthe Association of Avian Veterinariansrsquo (AAV) positionpaper on the sale of unweaned birds specifies that the organ-isation ldquoSUPPORTS the conveyance of unweaned birdsbetween qualified parties who possess the necessary skillsof handfeeding in accordance with accepted aviculturalindustry practicesrdquo and ldquoOPPOSES the sale or transfer ofunweaned birds to individuals KNOWN not to possess thenecessary level of experience in accordance with acceptedavicultural industry practices [emphasis theirs]rdquo Althoughposition statements such as these are important in that theyrecognise potential problems and can raise awarenessamong the avian veterinary community the effect of veteri-nary position statements on the sale practices of birdbreeders and pet shop owners is unknownAs hand-feeding is a labour-intensive procedure there is aneconomic advantage to selling unweaned birds quicklythereby ensuring the sale and effectively shifting the hand-feeding burden to the purchaser Compliance with the AAVposition statement also requires that the seller has adequateknowledge of the risks involved in hand-feeding and has theability to assess the skill level of the purchaser The sellermust also be willing to risk losing a sale or incurring theprolonged cost of caring for the unweaned bird if the sale isdelayed or refusedAlthough 15 states prohibit the sale of some unweanedanimals most limit the restriction to puppies and kittens


270 Engebretson

under the age of 8 weeks (some states also prohibit the saleof rabbits chicks [chickens] and ducks under a certain age)California recently became the first state to regulate the saleof unweaned birds in retail venues The new law requiresthat hand-fed birds be weaned prior to removal from theretail venue including pet shops bird marts and swapmeets The law further requires that pet shops that houseunweaned birds employ one or two individuals who havecompleted the Pet Industry Joint Advisory Councilrsquos hand-feeding certification course The bill was drafted andsponsored by the Animal Protection Institute

Welfare of othersThere is no doubt that many people enjoy parrots ascompanion animals and are attracted to parrots for variousreasons including companionship entertainment theirlsquopersonalityrsquo and their intelligence and vocal ability(Laughlin amp Dowrick 1987 Kid amp Kid 1998) Like othercommonly kept companion animals pet parrots may fillsome social esteem and cognitive needs of their humancaretakers (Laughlin amp Dowrick 1987 Kid amp Kid 1998)Schuppli and Fraser (2000) explained that ldquospecies may beill-suited as companion animals simply because they havequalities that may detract from or fail to enhance thewelfare of the ownerrdquo Examples include risk of physicalinjury inflicted on the owner or others by the animal orexposure and transmission of zoonotic diseases that mayhave an impact on people domestic animals or wildlife

Risk of physical injury and disease transmissionParrots of all species can inflict painful bites capable ofbreaking the skin and leaving scar tissue Larger birds suchas macaws and cockatoos are capable of inflicting seriousflesh wounds capable of leaving permanent disfigurementBiting is part of a parrotrsquos natural behaviour used toestablish dominance within a flock to defend territory or inresponse to frustration fear sexual aggression or play(Athan 1993) Nearly every parrot will experiment withbiting his or her human caretaker the behaviour can be rein-forced or discouraged depending on the knowledge andreaction of the caretaker Aggressive behaviour in manyspecies of parrots accompanies sexual maturity and attacksmay be spontaneous or may be accompanied by subtlewarning signs that can be difficult to detect by the inexperi-enced observer (Athan 1993) Although sexual aggression isreduced or eliminated in mammalian species kept ascompanions through the routine procedure of spaying andneutering no equivalent procedure currently exists for petbirds (Clubb 1998) Clubb (1998) noted that the adult repro-ductive stage is the longest life stage of a parrot and thatldquosexual maturity and resultant behavioural changes areinevitable in pet birds Bonding (pair formation) with asingle person displaced aggression sexual frustration anddestructive behaviour are among behavioural changes thatmany render birds undesirable companionsrdquoThere are many books available written by lay behaviouristsdescribing behaviour modification techniques that can beapplied with varying levels of success to help maintain pet

quality during the long sexually reproductive life stage ofparrots (Clubb 1998) Avian behavioural consultants arealso available in some areas to assist parrot caretakers inaddressing the behavioural problems that accompany sexualmaturity

Disease transmissionAvian chlamydiosis (C psittaci) commonly known as psit-tacosis or lsquoparrot feverrsquo can be transmitted through the airfrom birds to humans Although psittacosis has the potentialto infect any bird species it is particularly common inparrots pigeons and doves (Flammer 1997) The vastmajority of cases reported to the Centers for DiseaseControl (between 30 and 100 cases per year) result fromexposure to pet birds (CDC 1998) Psittacosis can causesignificant illness especially for people with compromisedimmune systems but most persons respond to oral anti-bacterial treatments (CDC 1998) Considering that millionsof birds are kept as pets the incidence of this disease inhumans is quite low The risks to the non-bird-owningcommunity are also quite low unless infected birds whichcan be asymptomatic carriers for many years and intermit-tently shed the bacteria are housed for public display orsaleThe importation of wild-caught birds significantly increasesthe disease risks associated with the pet bird trade Themixing of birds from different geographical ranges coupledwith close confinement and highly stressful conditionsincreases the susceptibility of imported birds to infectiousorganisms Pearson et al (1975) found in birds tested in US quarantineprior to the passage of the WBCA that 25 of groups ofbirds tested positive for Exotic Newcastle Disease (END)Parrots represented over 75 of the positive individualsAccording to F Dustan Clark Extension Poultry HealthVeterinarian at the University of Arkansasrsquos Avian Adviceeradication costs associated with exotic poultry diseaseoutbreaks in the US typically cost about $1 million per dayof the outbreak (Clark 2003)Schuppli and Fraser (2000) also noted that ldquooffensivequalities of animals (noise odour unruly or destructivebehaviour) may also be undesirable to owners mdash andpossibly other members of the communityrdquo As discussedabove many people eventually seek to rid themselves of theresponsibility of caring for their parrots (seelsquoRelinquishmentrsquo) The behavioural changes thataccompany developmental stages in the lives of parrots areoften cited as a primary challenge to the human-parrot rela-tionship (Wilson 1998 Clubb 1998) Wilson (1998) notedthat ldquoUnder the best of circumstances parrots are difficultcreatures to live with and few people will actually enjoylong-term cohabitation with themrdquo

Welfare of the environmentSchuppli and Fraserrsquos (2000) final consideration inassessing the suitability of companion animals addressesenvironmental impacts Issues to consider in this sectioninclude ecological impacts if the animal escapes or is



released adequate trade and collection regulation forspecies that exist in the wild risks of wild-capture on nativepopulations or ecosystems and whether or not such riskscan be addressed by captive breeding (Schuppli amp Fraser2000) I will examine each of these issues in turn

Ecological impacts of released or escaped parrots Released or escaped pet parrots can establish naturalised1

colonies and it is feared that some could become harmfullyinvasive pest species adversely impacting native wildlifeandor agriculture (Fisk amp Crabtree 1974 Shelgren et al1975) At least 74 free-living exotic parrot species havebeen reported in North America and at least 19 species havenested in Florida and southern California (Jackson 2003)There is considerable debate about the current andorpotential impacts of naturalised parrots on native wildlifespecies among scientists aviculturists birders environmen-talists and animal advocates (Engebretson 2004) Howeverfurther research is needed to provide relevant informationon this topic followed by further discussion about appro-priate measures to mitigate any identified impacts

Risks of wild capture on parrot populationsNearly one-third of the worldrsquos approximately 330 extantparrot species are threatened with extinction due to thecombined forces of habitat destruction and continuedcollection for the pet trade (Collar amp Juniper 1992) Thetrade in wild parrots seems to be driven by market demandcoupled with the large profits to the pet industry and thepoverty in many rural areas in many countries with wild-parrot populations (Wright et al 2001)Perhaps the single most effective tool against organisedpoaching wildlife smuggling and over-utilisation ofwildlife is the Convention on International Trade inEndangered Species of Wild Fauna and Flora (CITES)CITES was first signed into law in 1973 in order to protectcertain species of wild fauna and flora against over-exploitation through commercial trade The US adopted thetreaty in 1975 and the Endangered Species Act is itsenabling legislation Under CITES the trade in live or deadwildlife and their body parts is restricted or even prohibitedfor species listed in CITESrsquo three appendices which arebased on the level of endangerment of species Trade inspecies threatened with extinction is prohibited underAppendix I and monitored to varying degrees under theother two Appendices Specifically CITES prohibits theimport of Appendix I species for lsquocommercial purposesrsquounless the animal was specifically bred in captivity for thatpurposeThe US WBCA of 1992 provides further protections to wildbirds traditionally imported as companion animals forAmericans Congress found that the international pet trade

in wild-caught exotic birds contributes greatly to the declineof species in the wild and also that the trade produces anunacceptably high rate of mortality among the importedanimals The Act requires documentation by the importer onthe source of the bird a complete description and thereasons for import Also the importer is permitted to importonly two exotic birds as companion animals per year TheDepartment of the Interior administers the Act through theFish and Wildlife Service Wright et al (2001) revealed thatthe WBCA cut poaching rates from almost 50 to 20refuting the claims of some aviculturists (Desborough 1996)that limiting legal trade intensifies illegal trade andpoaching (Wright et al 2001)Although the concept of a legal trade in parrots managedunder a lsquosustainable harvestrsquo regime has been suggested asa potential conservation approach (Snyder et al 2000Beissinger 2001) and is in fact specifically listed as anexception under the WBCA to date no successful sustain-able harvest project has been demonstrated (Snyder et al2000) In 2003 however Argentina submitted a sustainableharvest proposal to the US Fish and Wildlife Service in thehope of exporting wild-caught blue-fronted Amazons(Amazona aestiva) harvested through the programme Thedecision on the permit is still pending and has been opposedby 93 scientists with expertise in parrot biology and bynumerous animal welfare organisations concerned that thetrade will be unsustainable andor will compromise thewelfare of individual parrotsSustainable harvest seems to hold little promise as aneffective conservation tool There is a documented relation-ship between legal and illegal international trade with thelegal trade providing a smokescreen behind which poachersoperate (Wright et al 2001) Currently there is no markingsystem that could reliably distinguish legally collected birdsfrom illegally collected birds (Beissinger 2001) In theabsence of reliable marking systems and tight controlsattempts at implementing sustainable harvest programmescould actually increase conservation problems rather thansolve them (Beissinger 2001)Despite the protections afforded by CITES and the WBCAthe international and domestic bird trade continues to be amajor threat for many species (Collar amp Juniper 1992)Enforcement of international and local laws continues to bea major conservation challenge especially in areas whereillegal practices are viewed as socially acceptable at thelocal level (Snyder et al 2000)

Captive breedingCaptive breeding might have the potential to reducepressures on wild populations by reducing the profitabilityof wild capture (Snyder et al 2000) However the cost ofwild capture tends to be much less than captive breeding(Snyder et al 2000) Indeed the demand for and subsequentcollection of wild parrots for the global pet trade continuesto threaten wild parrots despite the ability to producecaptive-bred birds (Wright et al 2001) The yellow-headedAmazon parrot for example has suffered the greatestdecline of any bird in the Americas mdash over 90 since the


1 The term lsquonaturalisedrsquo is used in accordance with the terminolo-gy outlined in Holmes and Stroud (1995) where lsquonaturalisedrsquo refersto an established population of organisms that have not beendomesticated and lsquoferalrsquo refers to an established population oforganisms that have been domesticated

272 Engebretson

1970s with the majority of the decline (68) in the last10 years (Michels 2002) This decline has continued despitethe wide availability of captive-reared yellow-headedAmazons for pet purposes It also unclear whether the avail-ability of inexpensive captive-bred birds would result infewer birds being captured for the trade or would merelyresult in a greater number of individuals acquiring birds aspets with no real reduction in the total number of wild-caught birds entering the pet tradeOne of the most common assertions made by private avicul-turists and pet parrot owners is that captive breedingcontributes to conservation of the species (Clubb 1992Desborough 1996) In reality breeding birds in captivitycontributes little or nothing to conservation efforts becausemost captive breeding is done outside official speciessurvival plans or other directed conservation efforts(Derrickson amp Snyder 1992 Snyder et al 2000 Gilardi2001 Wright et al 2001) Even if mutations are not specifi-cally selected for the moment the first generation isproduced (F1 generation) a breeder has been involved toone degree or another in a process whereby lsquonaturalselectionrsquo no longer applies thus the birds are divergingfrom whatever they were (or are) in the wild Invariablyselection factors begin to shift from factors that enable abird to survive in the wild to factors that enable a bird tosurvive in captivity so that the release of captive-bred birdsmay reduce the fitness of wild populations (Derrickson ampSnyder 1992 Ford 2002)It has been suggested that captive birds may support conser-vation efforts by serving as lsquoambassadorsrsquo thus generatingfunds for conservation efforts (Gilardi 2001) There is alack however of behavioural research demonstrating anassociation between viewing animals in a captive settingand either knowledge about the animal or intention to takeaction to conserve the animal in the wild In The ModernArk (1997) Vicki Croke noted that zoo visitors spend onaverage 3 min or less viewing each exhibit and typically donot read informational signs and McGovern (2002) notedthat although zoos around the world receive close to $10billion annually in revenue less than one-tenth of onepercent goes to conservation efforts It is unclear whatfactors inspire the public to support conservation efforts orwhat impact such support has on the conservation of thespecies in the wild For example despite a long history ofpublic display in zoos and travelling shows tiger popula-tions in the wild continue to dwindle whereas blue rightand humpback whales have received a high level of publicsupport for conservation efforts despite the fact that thesespecies have never been held in captivity

Discussion and conclusionsThe concept of companion animal lsquosuitabilityrsquo as discussedhere takes into account animal welfare ecological andsocietal considerations and holds implications for shapingpublic opinion and creating public policy This review hasexamined the available scientific evidence relating to thewelfare of captive parrots and examined other variablesaimed at evaluating the suitability of parrots as companion

animals In essence Schuppli and Fraser (2000) outlinedthat ethical objections to keeping a companion animal ariseif benefits to the owner are achieved to the detriment of theanimal if the animal poses a heath or safety risk to theowner or the community or if the acquisition or possessionof a particular species poses a risk to the environmentMany people enjoy keeping parrots as companion animalsindeed birds (including finches and canaries) are the fourthmost popularly kept companion animals in the US (Kid ampKid 1998 Meyers 1998) Even when bred in captivityexotic parrots are not considered domesticated animals andas such they retain the inherent behavioural and physicalneeds of wild parrots (Davis 1998 Graham 1998)However enclosures and housing arrangements for captiveparrots held by private owners are typically designed for theconvenience of the possessor not the needs of the animal(Graham 1998 van Hoek amp ten Cate 1998) and the restric-tions imposed by the captive environment may significantlyreduce the ability of the animal to express natural behaviourincluding socialisation foraging behaviour and flight(Sargent amp Keiper 1967 Keiper 1969 Graham 1998) Therestriction of natural behaviour may lead to stereotypicbehaviour an indication of poor welfare (Sargent amp Keiper1967 Keiper 1969 Mason 1991 King 1993 Broom 1996Graham 1998 van Hoek amp ten Cate 1998 Garner et al2003b Meehan et al 2003a 2004 Meehan et al 2003b)Many natural parrot behaviours especially those expressedafter sexual maturity may lead to a reduction in benefits ofparrot ownership for the caretaker and a reduction in qualityof care provided to the bird andor abuse abandonment orrelinquishment of the bird The trade in parrots as pets nega-tively impacts wild populations and jeopardises the welfareof individual wild-caught birds (Snyder et al 2000 Wrightet al 2001 Michels 2002)Schuppli and Fraser (2000) developed a classificationsystem of five categories based on the degree of suitabilityof animal species as companion animals Parrots were notspecifically mentioned or listed under any one categorydescribed by the two authors Based on the above evalua-tion parrots seem to fall between categories C and E but donot fit neatly into any one categoryAt first glance it appears that parrots belong in category Cwhich is described as follows ldquoSpecies that have complexor demanding requirements needing skillful and knowl-edgeable owners who are prepared to commit significanttime andor resources to animal ownership but whereownership is unproblematic with regard to procurementtransportation and effects on the community and the envi-ronment Control of ownership (eg ownership by onlyqualified persons) may be appropriate for such speciesrdquo(Schuppli amp Fraser 2000)However the lack of species-specific dietary information(Harrison 1998 Reid amp Perlberg 1998) the tendency forbird owners not to seek veterinary care (AmericanVeterinary Medical Association 2002) and the unknownimpact of released non-native parrots suggest that parrotsmight belong to category D defined as ldquoSpecies where



there is insufficient knowledge (eg regarding procurementtransportation environmental impact or the animalrsquos needs)to allow a confident assessment of its suitability as acompanion animal Use of these species might be accept-able in the future if knowledge becomes adequate and anynecessary safeguards are in placerdquo (Schuppli amp Fraser2000)Placing parrots in either category C or D however fails toaccount for the considerable environmental impacts of thewild bird trade which are directly linked to the demand anddesire for parrots as pets Considering the welfare of theenvironment most parrot species (particularly those whosewild counterparts are still traded) would fall under categoryE mdash ldquoSpecies that are unsuitable as companion animalsbecause of undue harm or risk to one or more of the animalthe owner the community or the environmentrdquo The authorsfurther explained that category E animals include ldquolong-lived species whose lifespan is likely to exceed an ownerrsquosability to provide carerdquo and ldquospecies whose requirements(eg for normal social behaviour) cannot reasonably be metin captivityrdquo (Schuppli amp Fraser 2000) As parrots are long-lived flight-adapted flock animals that have been comparedto primates and human toddlers in the needs of their socialand emotional lives it may be argued that they fit thecriteria for being deemed a category E animalUnfortunately retail pet shops typically sell parrots withlittle or no screening or training of prospective caretakersand place an emphasis on the sale of juveniles or unweanedbabies because a parrotrsquos lsquopet qualityrsquo is highest prior toreaching sexual maturity (Clubb 1998) Retail pet shopsappear to regard and treat parrots as category A or Banimals categories assigned to mice and hamsters and dogsand cats respectively by Schuppli and Fraser (2000)In contrast avian rescue organisations typically adopt outadult birds and require that prospective adopters agree to anapplication process complete with parrot care and behav-ioural training courses home inspections and follow-upconsultations prior to receiving a companion parrot Infollowing such a protocol avian rescues are effectivelylsquocontrolling the ownershiprsquo of birds in their care by essen-tially limiting ownership to lsquoqualifiedrsquo caretakers thusfollowing the recommendation set forth under Schuppli andFraserrsquos (2000) category CAs behaviour and care requirements vary between species itmay be appropriate to evaluate each parrot species sepa-rately or to divide parrot species into groups based on sizesmall-sized parrots such as budgerigars (Melopsittacusundulatus) cockatiels (Nymphicus hollandicus) andlovebirds (Agapornis spp) medium-sized parrots such asconures (Aratinga spp) Amazons (Amazona spp) andAfrican grey parrots (Psittacus erithacus) and large-sizedparrots such as cockatoos (Cacatua spp) and macaws (Araspp) It is important to note however that although smallerbirds in general should be easier to care for in terms ofmeeting environmental needs the relatively low cost ofthese species may mean that they are at an increased risk of

being purchased on impulse or as a childrsquos pet Their lowercommercial value may also place them at a greater risk ofbeing considered lsquodisposablersquo when no longer wanted by acaretaker or when necessary veterinary care exceeds theretail value of the animal (Low 2000) Thus smaller birdsmay face different challenges in the pet trade but not neces-sarily fewer challenges than their larger higher priced coun-terpartsMany animal advocates believe that regulation of the acqui-sition sale and relinquishment of animals kept as compan-ions could improve animal welfare (Rollin amp Rollin 2003)especially for animals that require specialised care(Schuppli amp Fraser 2000) However regulations protectingcaptive birds from inappropriate care acquisition and salesare sorely lacking at the federal and state level (AnimalProtection Institute 2005)In welfare assessments it is important to take account ofindividual variation in response to situations or environ-mental conditions (Broom 1996) Despite the difficulty ofcare and potential for the development of stereotypic behav-iours aggression and injury there appear to be someparrotndashhuman relationships in which both the caretaker andthe animal experience good welfare It has also beensuggested that basic obedience training for parrots and theircaretakers can improve the welfare of captive parrots(Glendell personal communication 2004) thereby increasingan individual birdrsquos compatibility in a home environmentEvidence suggests however that as long as the privateownership of parrots remains socially acceptable andcommercial profits persist the smuggling of parrots for thepet trade will probably continue despite trade restrictionsand availability of captive bred birds (Snyder et al 2000)Therefore finding ways to replace the demand for parrots aslsquopetsrsquo with a demand for preserving the species in the wildmay be the best way to reduce captive parrot welfareproblems and ensure the welfare of wild parrots and theenvironment

Acknowledgements Many thanks to Karen Hirsch Dena Jones Barry KentMacKay and Nicole Paquette for invaluable discussion onthis topic and for helpful comments on earlier versions ofthis paper

ReferencesAengus WL and Millam JR 1999 Taming parent-rearedorange-winged Amazon parrots by neonatal handling Zoo Biology18 177-187Altman RB 1998 Twenty years of progress in avian anaesthesiaand surgery Journal of the American Veterinary Medical Association21(8) 1233-1235American Veterinary Medical Association 2002 US PetOwnership and Demographics Sourcebook (2002 Edition) AmericanVeterinary Medical Association Membership and Field ServicesIllinois USAAnimal Protection Institute 2005 Current law and suggestedapproaches to improving captive bird welfarehttpwwwapi4animalsorgb4a2_birdwelfarephp


274 Engebretson

Association of Avian Veterinarians (AAV) Position on thesale of unweaned birds httpwwwaavorgUnweanedhtm(accessed 5 May 2006)Athan MS 1993 Guide to a Well-Behaved Parrot BarronsEducational Series New York USABeissinger SR 2001 Trade of live wild birds potential principalsand practices of sustainable use In Reynolds J Mace GM RedfordKH and Robinson JG (eds) Conservation of Exploited Species pp 182-202 Cambridge University Press Cambridge UKBirchall A 1990 Whorsquos a clever parrot then New ScientistFebruary 24 38-43Blanchard S 1999 Common parrot behavioural myths andwhy they are myths httpwwwcompanionparrotcomCommon20Parrot20Behaviorial20Mythshtm (accessed 5May 2006)Blanchard S 2001 The poultrification of parrotshttpwwwcompanionparrotcomPoultrification20of20Parrotshtm (accessed 5 May 2006)Blood DC and Studdert VP 1988 Bailleirersquos ComprehensiveVeterinary Dictionary p 653 Bailliere Tindall London UKBrodnick PS Thayer BA and Ritchie W 1994 Feather pick-ing disorder and trichotollomania an avian model of human psy-chopathology Journal of Behaviour Therapy and ExperimentalPsychiatry 25 189-196Broom DM 1996 Animal welfare defined in terms of attempts tocope with the environment Acta Agriculturae Scandinavica SectionA Animal Science Suppl 27 22-28Bucher EH Carlos ST Miglietta S and Zaccagnini MA1992 Status and management of the blue-fronted Amazon parrotin Argentina PsittaScene 4(2) 3-6Centers for Disease Control and Prevention (CDC) 1998Compendium of measures to control Chlamydia psittaci infection amonghumans (psittacosis) and pet birds (avian chlamydiosis) 47(RR10)httpwwwcdcgovmmwrpreviewmmwrhtml00053877htm(accessed 5 May 2006)Clark FD 2003 Exotic poultry diseases an updateh t t p w w w t h e p o u l t r y s i t e c o m F e a t u r e d A r t i c l e FATopicaspAREA=HealthAndWelfareampDisplay=98 (accessed 5May 2006)Clubb SL 1992 The role of private aviculture in the conservationof Neotropical psittacines In Beissinger SR and Snyder NFR (eds)New World Parrots in Crisis Solutions from Conservation Biologypp 117-131 Smithsonian Institute Press Washington DC USAClubb SL 1998 Captive management of birds for a lifetimeJournal of the American Veterinary Medical Association 21(8)1243-1245Collar NJ and Juniper AT 1992 Dimensions and causes of theparrot conservation crisis In Beissinger SR and Snyder NFR (eds)New World Parrots in Crisis Solutions from Conservation Biology pp 1-24 Smithsonian Institute Press Washington DC USACollette JC Millam JR Klasing KC and Wakenell PS 2000Neonatal handling of Amazon parrots alters the stress responseand immune function Applied Animal Behaviour Science 66 335-349Croke V 1997 The Modern Ark The Story of Zoos Past Present andFuture BardAvon Books New York USADavis C 1998 Appreciating avian intelligence the importance ofa proper domestic environment Journal of the American VeterinaryMedical Association 212(8) 1220-1222

Derrickson SR and Snyder NFR 1992 Potentials and limits ofcaptive breeding in parrot conservation In Beissinger SR andSnyder NFR (eds) New World Parrots in Crisis Solutions fromConservation Biology pp 133-163 Smithsonian Institute PressWashington DC USADesborough L 1994 Breeder news and views Bird Breeder66(10) 64-65Desborough L 1996 Breeder news and views Bird Breeder68(4) 6-7Donoghue S 1997 Nutrition of companion birds and reptilesProceedings from the 21st Annual WalthamndashOSU Symposium for theTreatment of Small Animal Diseases Exotics pp 27-33 College ofVeterinary Medicine Ohio State University Ohio USADuncan IJH 1996 Animal welfare defined in terms of feelingsActa Agriculturae Scandinavica Section A Animal Science Suppl27 29-35Eifert J Tarpley HL and Latimer KS 2003 Study case mdashaspergillosis in a blue-fronted Amazon parrot (Amazona aestiva)

httpwwwvetugaeduvppclerkeifert (accessed 5 May 2006)Engebretson M 2004 For the birds Animal Issues 35(1) 14-15Farm Animal Welfare Council (FAWC) 1992 FAWCupdates the five freedoms The Veterinary Record 131 357Field DA and Thomas R 2000 Environmental enrichmentfor psittacines at Edinburgh Zoo International Zoo Yearbook37 232-237Fisk LH and Crabtree DM 1974 Black-hooded parakeet newferal breeding species in California American Birds 28 181-195Flammer K 1997 Update on avian chlamydiosis In Proceedingsfrom the 21st Annual WalthamndashOSU Symposium for the Treatment ofSmall Animal Diseases Exotics pp 15-18 College of VeterinaryMedicine Ohio State University Ohio USAFlammer K 1998 Twenty years of progress in pet birdresearch Journal of the American Veterinary Medical Association21(8) 1231-1233Forbes NA and Glendell G 1999 Wing clipping in psittacinebirds The Veterinary Record 144 299 (letter)Ford MJ 2002 Selection in captivity during supportive breedingmay reduce fitness in the wild Conservation Biology 16(3) 815-825Forshaw JM 1973 Parrots of the World Doubleday New YorkUSA Cited in Schuppli CA and Fraser D 2000 A framework forassessing the suitability of different species as companion animalsAnimal Welfare 9 359-372Fraser AF and Broom DM 1990 Farm Animal Behaviour andWelfare 3rd Edition Bailliere Tindall London UKGarner JP Mason GJ and Smith R 2003a Stereotypic route-tracing in experimentally caged songbirds correlates with generalbehavioural disinhibition Animal Behaviour 66 771-727Garner JP Meehan CL and Mench JA 2003b Stereotypies incaged parrots schizophrenia and autism evidence for a commonmechanism Behavioural Brain Research 145 125-134Gilardi J 2001 Breeding parrots for conservation an idea whosetime has come or come and gone PsittaScene13(2) 12-13Gilardi JD and Munn CA 1998 Patterns of activity flockingand habitat use in parrots or the Peruvian Amazon The Condor100 641-653Gill FB 1990 Ornithology 2nd Edition WH Freeman andCompany New York USA



Graham DL 1998 Pet birds historical and modern perspectiveson the keeper and the kept Journal of the American VeterinaryMedical Association 212(8) 1216-1219Harcourt-Brown N 2003 Incidence of juvenile osteodystrophyin hand-reared grey parrots (Pissacus e erithacus) The VeterinaryRecord 152 438-439Harcourt-Brown N 2004 Development of the skeleton andfeathers of dusky parrots (Pinous fuscus) in relation to their behav-iour The Veterinary Record 154 42-48Harris DJ 1997 Psittacine pediatric husbandry In Proceedingsfrom the 21st Annual WalthamndashOSU Symposium for the Treatment ofSmall Animal Diseases Exotics pp 23-24 College of VeterinaryMedicine Ohio State University Ohio USAHarrison GJ 1998 Twenty years of progress in pet bird nutri-tion Journal of the American Veterinary Medical Association 212(8)1226-1230Held S Mendl M Devereux C and Byrne RW 2001 Studiesin social cognition from primates to pigs Animal Welfare 10Suppl S209-S217Hesterman H Gregroy NG and Boardman WSJ 2001Deflighting procedures and their welfare implication in captivebirds Animal Welfare 10 405-419Holmes JS and Stroud DA 1995 Naturalised birds feral exot-ic introduced or alien British Birds 88 602-603 (letter)Jackson J 2003 Pandorarsquos birds Birderrsquos World October 200355-59Kearns KS 2003 Avian aspergillosis Recent advances in avian infectiousdiseases International Veterinary Information Service Ithaca NY USAhttpwwwivisorgadvancesKearnskearns2ivispdf (accessed 5 May2006)Keiper RR 1969 Causal factors of stereotypies in caged birdsAnimal Behaviour 17 114-119Kid AH and Kid RM 1998 Problems and benefits of bird own-ership Psychological Reports 83 131-138King CE 1993 Environmental enrichment is it for the birds ZooBiology 12 509-512King CE 2000 Situation-dependant management of large parrotsby manipulation of the social environment International ZooYearbook 37 238-244Knights P and Currey D 1990 Will Europe ban wild-birdimports Defenders NovDec 20-25Laughlin CA and Dowrick PW 1987 Psychological needs filledby avian companions Anthrozoos 6(3) 166-171Lightfoot TL 2002 Avian behaviour Hartz Exotic HealthNewsletter 1 4Low R 2000 Over-production of parrots giant implications forparrot welfare PsittaScene 12(3) 12-13Mabb KT 2002 Naturalized (wild) parrots in California a current assess-ment Department of Biological Sciences California State PolytechnicUniversity Pomona CA USA httpnaturealiorgparrot_projectmabb_tgf_proceedingshtm (accessed 5 May 2006)Mason GJ 1991 Stereotypies a critical review Animal Behaviour41 1015-1037May D and Hovetter V 2002 Where the Wild Greys Are A Dayin the Life of Africarsquos Grey Parrots VHS World Parrot TrustGlamor House Hayle Cornwall TR7 4HY UKMcCluggage D and Higdon PL 1999 Holistic Care for Birds AManual of Wellness and Healing IDG Books Worldwide NewYork USA

McGovern K 2002 Call of the wild ParrotChroniclescom (RareSpecies Conservatory Foundation) Summer 2002 httpwwwpar-rotchroniclescomsummer2002conservationwatchhtm(accessed 5 May 2006)Meehan CL Garner JP and Mench JA 2003a Isosexual pairhousing improves the welfare of young Amazon parrots AppliedAnimal Behaviour Science 81 73-88Meehan CL Garner JP and Mench JA 2004 Environmentalenrichment and development of cage stereotypy in orange-wingAmazon parrots (Amazona amazonica) DevelopmentalPsychobiology 44 209-218Meehan CL Millam JR and Mench JA 2003b Foraging oppor-tunity and increased physical complexity both prevent and reducepsychogenic feather picking by young Amazon parrots AppliedAnimal Behaviour Science 80 71-85Meyers NM 1998 Perspectives on pet bird welfare from the petindustry Journal of the American Veterinary Medical Association212(8) 1238-1242Michels A 2002 Parrot smuggling still a global problem Animal WelfareInstitute Quarterly 51(4) httpwwwawionlineorgpubsQuarterlyfall02par-rothtm (accessed 5 May 2006)Millam JR Kenton B Jochim L Braownback T and BriceAT 1995 Breeding orange-winged Amazon parrots in captivityZoo Biology 14 275-284Nimon AJ and Broom DM 1999 The welfare of farmed mink(Mustela vison) in relation to housing and management a reviewAnimal Welfare 8 205-228Pearson JE Senne DA Carbrey EA Erickson GA andMiller LD 1975 Viral isolations from exotic birds offered forimportation into the United States Proceedings of the AnnualMeeting of the United States Animal Health Association 1975 (79)219-223Pepperberg IM 1999 The Alex Studies Cognitive andCommunicative Abilities of Grey Parrots Harvard University PressCambridge MA USA London UKPepperberg IM 2004 Cognitive and communicative capacities ofgrey parrots implications for the enrichment of many speciesAnimal Welfare 13 Suppl S203-S208Reid BR and Perlberg W 1998 Emerging trends in pet birddiets Journal of the American Veterinary Medical Association 21(8)1236-1238Ritchie BW 1997 Diagnosing and preventing common viralinfections in companion birds In Proceedings from the 21st AnnualWalthamndashOSU Symposium for the Treatment of Small AnimalDiseases Exotics pp 7-13 College of Veterinary Medicine OhioState University Ohio USARitchie BW Gregory CR Latimer KS Pesti DCampagnoli R and Luckert PD 2000 A review of the mostcommon viruses affecting Psittaciformes International ZooYearbook 37 257-273Rollin BE and Rollin MDH 2003 Dogmaticisms and cate-chisms ethics and companion animals In Armstrong SJ andBotzler RG (eds) The Animal Ethics Reader pp 504-509Routledge New York USARomagnano A 2003a Parrot preventive medicine Proceedingsof the International Aviculturists Society httpwwwfunny-farmexoticscomIAS2003ProceedingsRomagnano_Preventativepdf (accessed 3 May 2006) Romagnano A 2003b Problems associated with improper hand-feeding Hartz Exotic Health Newsletter 2 3


276 Engebretson

Sargent TD and Keiper RR 1967 Stereotypies in cagedcanaries Animal Behaviour 15 62-66Schuppli CA and Fraser D 2000 A framework for assessingthe suitability of different species as companion animals AnimalWelfare 9 359-372Seibert LM Crowell-Davis SL Wilson GH and RitchieBW 2004 Placebo-controlled clomipramine trial for the treat-ment of feather picking disorder in cockatoos Journal of theAmerican Hospital Association 40 261-269Shelgren JH Thompson RA Palmer TK Keffer MOClark DO and Johnson J 1975 An Evaluation of the Pest Potentialof the Ring-Necked Parakeet Nanday Conure and the Canary-WingedParakeet in California California Department of Food andAgriculture Division of Plant Industry Special Services UnitSacramento USASnyder N McGowan P Gilardi J and Grajal A 2000 ParrotsStatus Survey and Conservation Action Plan 2000ndash2004 InternationalUnion for Conservation of Nature and Natural Resources GlandSwitzerland Cambridge UKStamps J Kus B Clark A and Arrowood P 1990 Social rela-tionships of fledgling budgeriars Melopsitticus undulates AnimalBehaviour 40 688-700

van Hoek CS and ten Cate C 1998 Abnormal behaviour incaged birds kept as pets Journal of Applied Animal Welfare Science1(1) 51-64Voren H 1995 Wild child Bird Breeder Magazine Breeder Q ampA November httpwwwvorencom95-11htm (accessed 5May 2006)Vriends MM 1996 Hand-Feeding and Raising Baby Birds BarronsEducational Series New York USAWilson LH 1998 Considerations in selecting an appropriate petbird Journal of the American Veterinary Medical Association 212(8)1222-1225Wobeser GA 1994 Investigation and Management of Disease inWild Animals Plenum Press New York USAWright TF Toft CA Enkerlin-Hoeflich E Gonzalez-Elizondo J Albornoz M Rodriguez-Ferraro A Rojas-Suarez F Sanz V Trujillo A Beissinger SR BerovidesVA Galvez AX Brice AT Joyner K Eberhard J Gilardi JKoenig SE Stoleson S Martuscelli P Meyers JM RentonK Rodriguez AM Sosa-Asanza AC Vilella FJ and WileyJW 2001 Nest poaching in neotropical parrots ConservationBiology 15 710-720


264 Engebretson

Review approachSchuppli and Fraser (2000) developed a systematic analysisto evaluate the suitability of different species as companionanimals based on a wide range of issues such as thosedescribed above that are relevant to such an assessmentTheir analysis considered three main criteria the welfare ofthe animal the welfare of others (including humans andother animals) and the welfare of the environment Thispaper will review the current literature on the welfare ofcaptive birds and utilise the framework described bySchuppli and Fraser (2000) to assess the suitability ofparrots as companion animals

Welfare of the animalThe examination of animal welfare is a useful tool in deter-mining the suitability of keeping a particular species as acompanion animal This is because welfare describes thestate of an animal at a specific time and can be lsquogoodrsquo orlsquopoorrsquo regardless of what people think about the morality ofusing such animals in a particular wayThe lsquofive freedomsrsquo of the Farm Animal Welfare Council(1992) have been used to evaluate animal welfare for manyspecies and are used as part of the Schuppli and Fraser(2000) criteria for determining companion animal suit-ability These freedoms are (1) freedom from hunger thirstand malnutrition (2) freedom from disease and injury(3) freedom from physical and thermal discomfort(4) freedom from fear distress and other negative psycho-logical states and (5) freedom to carry out most normalforms of behaviour Although many of these freedoms areinter-related mdash for example deprivation of the freedom toexpress normal forms of behaviour may cause a negativepsychological state that results in physical injury mdash I willattempt to evaluate each freedom individually with theexception of the last two freedoms (4 and 5) which will bediscussed together

Freedom from hunger thirst and malnutritionThis first freedom is further defined as the animal havingldquoready access to fresh water and a diet to maintain fullhealth and vigourrdquo (Farm Animal Welfare Council 1992)Common captive parrot caging environments provide ampleaccess to both food and water so it would appear that inmost cases the first freedom is met However as Schuppliand Fraser (2000) have pointed out the nutritional require-ments of the species must be adequately known and suitablefoods must be available to the owner in order to assure ldquofullhealth and vigourrdquoIt has been estimated that malnutrition is responsible for upto 90 of all clinical conditions seen by avian practitioners(Harrison 1998) It is well recognised among avian profes-sionals that seed diets lack nutrients and are high in fathowever seed diets remain the most widely available andmost commonly fed pet bird diet (Harrison 1998 Reid ampPerlberg 1998)Although a number of high-quality formulated diets areavailable in the form of pellets dietary standards are rela-

tively non-existent and it is unlikely that detailed nutritionalrequirements will ever be documented for all the variousspecies of birds kept as pets (Harrison 1998 Reid ampPerlberg 1998) Despite this many labels give the impres-sion that the diet is complete when in fact the food containsonly minimum requirements which may not provide suffi-cient nutrition for some birds Further complicating mattersmany avian professionals recommend that birds not be feda pellet-only diet and that formulated pellet diets be supple-mented with fresh fruit and vegetables to ensure optimalnutrition and health (Reid amp Perlberg 1998) Many nutri-tional problems diagnosed in birds seem to arise fromconfusion on the part of the caretaker over conflicting infor-mation for achieving balanced nutrition (Donoghue 1997)

Freedom from disease and injuryThe existence of adequate veterinary knowledge and avail-ability is necessary for the fulfilment of this freedomDuring the past 20 years research by avian practitioners andacademics and the skills of avian veterinarians haveimproved considerably Speciality avian practices havetailored diagnostic tests emergency medical procedures andanaesthesia monitoring for birds (Altman 1998 Flammer1998) However despite the advances in avian veterinarymedicine and the availability of veterinarians specialising inavian care and treatment only 117 of bird-owning house-holds currently seek veterinary advice for their birds(American Veterinary Medical Association 2002)There are a number of viral bacterial fungal and parasiticdiseases that pet birds can become infected with but viralinfection is one of the major causes of mortality in parrots(Ritchie et al 2000) The four most common viral infectionsinfecting pet parrots are avian polyomavirus proventriculardilatation disease (PDD) psittacine beak and featherdisease (PBFD) and Pachecorsquos disease (Ritchie et al 2000)There is no cure for avian polyomavirus although there is areliable vaccine on the market and there is no known cureor vaccine for PBFD or PDD Although a vaccine forPachecorsquos disease (PsittimuneTM Biomune Company 8906Rosehill Road Lenexa KS 66215 USA) was registered bythe United States Department for Agriculture for use in petbirds in 1990 (Center for Veterinary Biologics 2005) it isnot routinely used except in the face of an outbreak(Romagnano 2003a) Some veterinarians have had successin treating birds in early stages of the disease withAcyclovir an anti-herpesvirus agent (Ritchie 1997)Avian chlamydiosis caused by Chlamydophila psittacicommonly known as psittacosis or lsquoparrot feverrsquo is one ofthe more common bacterial infections in birds and is trans-mittable to humans (see Welfare of others below) Birdswith mild infection may be asymptomatic carriers and mayshed the disease for many months or years with no outwardsign of illness The organism is shed in the faeces and nasaldischarge of infected birds is resistant to drying and canremain infectious for several months (Centers for DiseaseControl and Prevention [CDC] 1998) Severely ill birdsexhibit clinical signs of diarrhoea severe lethargy weightloss poor feather condition conjunctivitis nasal discharge








266 Engebretson









268 Engebretson













270 Engebretson

















272 Engebretson











274 Engebretson









276 Engebretson










266 Engebretson









268 Engebretson













270 Engebretson

















272 Engebretson











274 Engebretson









276 Engebretson








268 Engebretson













270 Engebretson

















272 Engebretson











274 Engebretson









276 Engebretson









270 Engebretson

















272 Engebretson











274 Engebretson









276 Engebretson













272 Engebretson











274 Engebretson









276 Engebretson










274 Engebretson









276 Engebretson








276 Engebretson




The welfare and suitability of parrots as companion animals: a review

Documents

Transcript of The welfare and suitability of parrots as companion animals: a review