L 162 - 2008-09 - Bilag 6: Henvendelse af 28/4-09 fra Anima om fremvisning af ikke-domesticerede dyr i cirkus

AbstractA comprehensive synopsis of the welfare of captive, wild (ie non-domesticated) animals in travelling circuses is missing. Weexamined circus animal welfare and, specifically, behaviour, health, living and travelling conditions. We compared the conditions ofnon-domesticated animals in circuses with their counterparts kept in zoos. Data on circus animals were very scarce; where datawere absent, we inferred likely welfare implications based on zoo data. Circus animals spent the majority of the day confined, about1–9% of the day performing/training and the remaining time in exercise pens. Exercise pens were significantly smaller thanminimum zoo standards for outdoor enclosures. Behavioural budgets were restricted, with circus animals spending a great amountof time performing stereotypies, especially when shackled or confined in beast wagons. A higher degree of stereotyping in circusesmay be indicative of poorer welfare. Inadequate diet and housing conditions, and the effects of repeated performances, can leadto significant health problems. Circus animals travel frequently and the associated forced movement, human handling, noise, trailermovement and confinement are important stressors. Although there is no conclusive evidence as to whether animals habituate totravel, confinement in beast wagons for long timeperiods is a definite welfare concern. Circuses have a limited ability to makeimprovements, such as increased space, environmental enrichment and appropriate social housing. Consequently, we argue thatnon-domesticated animals, suitable for circus life, should exhibit low space requirements, simple social structures, low cognitivefunction, non-specialist ecological requirements and an ability to be transported without adverse welfare effects. None of thecommonest species exhibited by circuses, such as elephants and large felids, currently meet these criteria. We conclude that thespecies of non-domesticated animals commonly kept in circuses appear the least suited to a circus life.

130 Iossaet alshould not be used in circuses” (Amboseli ElephantResearch Project 2007). Moreover, in addition to animalwelfare considerations, several species widely kept incircuses pose serious concerns in terms of risk to the public.The number of keepers and visitors injured or killedworldwide (1–11 per year during 1982–2004) by African(Loxodontaafricana)and Asian (Elephasmaximus)elephants in zoos (Goreet al2006) and captive tiger(Pantheratigris)attacks on people in USA circuses andtheme parks (1.75 fatal, 9 non-fatal attacks per year [Nyhuset al2003]) seem to represent a disproportionate threat inproportion to their number (360–720 times greater risk of afatal attack than a domestic dog [Nyhuset al2003]).Elephants and tigers are the main causes of occupationalfatalities for circus workers and zoo keepers in the USA(Langley & Hunter 2001).In this context, we examine the welfare of non-domesticatedanimals in circuses and the extent to which their lives differfrom other captive animals’ lives. We focus on European,and especially UK circuses as worldwide data are sparse andmainly available from non peer-reviewed literature. Weattempt to review all animals commonly kept in circusesworldwide but, inevitably, research has focused on a fewspecies which are best represented in our examples. Wheredata were lacking for some measures, we have reviewed theevidence available from studies of animals in other captivesituations, such as zoos and, secondarily, laboratories andfarms. Out of necessity, some of this literature includesdomestic animals. We believe this comparison to be valid fortwo reasons. Firstly, zoos keep all of the species commonlyused in circuses and, in both cases, the history of the animals(captive-bred or wild-caught, owned by one or several insti-tutions) is comparable. Secondly, despite being domesticatedand adapted to living with humans, domestic species are stillliable to experience negative welfare whenever the ability toperform highly-motivated behaviours, inherited from theirwild ancestors, is thwarted (eg Goodwin 1999; Schrøder-Petersen & Simonsen 2001; Cooper & Albentosa 2005). Forthese reasons, we think it reasonable to assume that anyshortfalls in the level of welfare of zoo, laboratory or farmanimals is equally, or more likely, to apply to other captivewild animals in similar situations. In this paper, we firstreview the number and origin of animals involved in thecircus industry. Following a framework initially developedto assess the suitability of exotic species as pets (Schuppli &Fraser 2000), we then examine whether non-domesticatedanimals are suited to living in circuses. In particular, wereview: (i) the welfare of non-domesticated animals incircuses (living and travelling conditions, behaviour, healthand performance) and, (ii) following this, drawing on theevidence collated, we assess whether non-domesticatedanimals are suited to a circus life.www.scholar.google.com), and the bibliography of signifi-cant reports (Cox 1998; Clubb & Mason 2002) followingthe methodology proposed by Pullin and Stewart (2006).We used the search terms (‘circus AND animal’, ‘PantheratigrisAND circus’, ‘tiger AND circus’, ‘primate ANDcircus’, ‘Elephas AND circus’, ‘Loxodonta AND circus’,‘elephant AND circus’). In addition, we searched theWorldwide Web to investigate travel habits of European andNorth American circuses using ‘circus AND touringschedule’, and ‘circus AND transport’ as search terms.

The numbers and origin of non-domesticatedanimals in circusesThere are two types of circuses: static and travelling. In thisreview, ‘circus’ refers to a travelling group of entertainersand animals. The animals are confined in ‘beast wagons’when travelling and for a certain period of time afterarriving at a location. Beast wagons are transport containersthat are typically small enough to be carried on a longtrailer. Alternatively, animals are held in exercise pens onsite (larger cages, connected to the beast wagon) when theyare not performing. When not on tour they are held at onelocation, such as winter quarters, but very little informationon these facilities is readily available, so we did not includethem in this review.The total number of animals kept in captivity in circusesworldwide is unknown; estimates (including domesticanimals) range from a minimum of 2,400 to a maximum of5,900 individuals in Europe (Galhardo 2005). In Britishcircuses, there were approximately 513 wild and domesticanimals in 1990 (Kiley-Worthington 1990); since then, thenumber of non-domesticated animals has declined from92 individuals recorded in 1997 to 33 in 2005 (Born FreeFoundation & RSPCA 2006) and to 47 in 2007 (Radford2007), perhaps partially due to the outbreak of foot-and-mouth disease in 2000–2001. In the period 1975–2005, thetotal number of animals officially exported globally forcircus and travelling exhibition purposes was about 25,500(Table 1). Of these, carnivores (31%), birds (27%) andreptiles (22%) represent about 80% of the trade, whilst themost traded species are tigers with 3,003 individuals, brownbears (Ursusarctos)with 1,866, pythons (Python spp) with1,808, macaques (Macaca spp) with 1,547, lions (Pantheraleo)with 1,473, lovebirds (Agapornis spp) with 1,283 andAsian elephants with 1,168. For some species, a consider-able number of non-domesticated individuals are housed incircuses. For instance, worldwide, about 31% of all captiveAfrican and Asian elephants are kept in circuses (althoughthis figure is based on a total that underestimates thenumber of working elephants in Asia, see Clubb & Mason[2002]). Some 800 captive tigers are involved in globalconservation strategies, whilst estimates of privately-ownedindividuals (including exotic pets and those in non-accred-ited zoos, circuses, and safari parks) vary between5,000 and 12,000 (Nyhuset al2003). This number is greaterthan the number of breeding individuals in the wild (CatSpecialist Group 2002) and is outside management forbreeding and reintroduction purposes.

A review of wild animals in travelling circuses 131Similarly, data on the origin of animals in circuses are veryscarce. Kiley-Worthington (1990) reported that 40% ofcarnivores and 14% of ungulates in 15 British circuses wereunwanted zoo animals, whereas approximately 94% ofelephants were wild-caught. However, it must be noted that,although the remaining animals were classified as bred incircuses, the category ‘circus’ actually included ‘privateowners, market, etc’ (Kiley-Worthington 1989a). Thisimplies that an unknown percentage of animals classified ascaptive-bred in circuses were actually bred in other privatefacilities.The International Tiger Studbook(Müller 2004)has no record of the numbers of tigers bred in zoos andsubsequently released to circuses, safari parks and privateowners before the age of three. Consequently, an unknownproportion of captive-born tigers pass into private hands(Müller 2004). The origin and lineage of the majority ofthese animals is unknown but, as some zoo associations donot allow member establishments to pass its animals tocircuses (eg BIAZA 2005), this source may be reduced insome countries. Thus, the contribution of circuses to captivebreeding conservation programmes is, at best, negligible.Table 1Convention on International Trade inEndangered Species of Wild Fauna and Flora (CITES)trade statistics on net export of all animal species official-ly traded worldwide for circus and travelling exhibitionpurposes in the period 1975–2005.TaxonCarnivoresFelidaeUrsidaeCanidaeReptiles and amphibiansSnakesLizards and geckosChameleonsCrocodilesTortoisesFrogsCetaceans and sealsPrimatesBirdsParrotsBirds of preyOtherHerbivoresElephantsOthersTotal1,64019825,5791,3413095,1191,8382,8271,1175168172811295082,8896,7695,4122,3481285,687Number of animals Sub-total7,888

ment), may enhance health and reproductive potential ofcaptive animals, and is recognised by zoo managers as auseful tool to improve captive species management(Desmond & Laule 1994). Training by means of negativereinforcement and/or punishment may be the cause of poorwelfare for the captive animal and can also establish a poorrelationship between trainer and animal (Siemoneit-Barum1995; Hemsworth & Barnett 2000). Kiley-Worthington(1990), during 200 h observation in British circuses,witnessed no signs of prolonged or acute distress. Some ofthe animals initially showed fear and anxiety beforebecoming accustomed to trainers; others showed frustrationand avoidance behaviours and refusal to perform certainacts (Kiley-Worthington 1990). The training observedincluded reducing levels of fear, positive reinforcement,infrequent negative reinforcement (the use of body postureand sticks or whips for controlling the animal’s movement)but no evidence of cruelty. However, not enough trainingwas practised, it lacked innovation and it was not alwaysappropriate for the species; overall, there were not enoughgood trainers (Kiley-Worthington 1989b, 1990).Performance acts in the presence of spectators may causesevere stress to non-domesticated animals. Loud noise is awell-known stressor in captive animals; acoustical stresswithin and outside the human hearing range can cause criticalalteration in physiological parameters (Stoskopf 1983; Bowles& Thompson 1996). Tigers may develop gastroenteritis as aconsequence of persistent, loud noise (Cociuet al1974). It has

cated animals and/or animals completely naïve to travel,show signs of behavioural and physiological distress whentravelling (eg Trunkfield & Broom 1990; Monteset al2004), even more than would be expected from physicalrestraint alone (López-Olveraet al2006). In contrast,domesticated animals accustomed to handling are generallyless stressed by being restrained and transported (review inGrandin 1997). To date, some studies suggest that circuselephants and tigers habituate to travel but, other than bodytemperature (Toscanoet al2001), only behaviouralmeasures are available (Nevill & Friend 2003; Williams &Friend 2003; Nevillet al2004). In a study on the transportenvironment in six USA circuses, only two circuses usedinsulated walls and high capacity ventilation fans tomaintain internal temperatures within a safe range (Toscanoet al2001). The elephants transported did not experiencetemperatures outside their normal range, butdrivers/handlers may be unaware of any critical temperatureincrease in the trailers as monitoring systems were absent.For elephants, movement in trailers is constrained becausethey are transported chained (Toscanoet al2001). In zootigers, pacing varies individually but altered cortisol levelspersist for 3–6 days after transport in animals with experi-ence of travelling (transported on at least two previousoccasions) and 9–12 days in naïve tigers, suggesting thattravelling is a stressful experience (Dembiecet al2004).Kiley-Worthington (1990) stated that British circus animalsappeared habituated to travel but that there was concern onwelfare grounds because the animals were confined in thebeast wagons for long periods. Domestic horses (Equuscaballus)are frequently transported for sport and recre-ational purposes; those that have positive travel experiences(ie loading, transport density, careful driving) seem tohabituate readily to travel but they are also likely to developproblems associated with frequent travel, such as fatigue,weight loss, restricted movement and disrupted feedingpatterns (Waran & Cuddeford 1995; Waranet al2002). Onthe other hand, many horses are transported throughout theirlives with few problems (Waranet al2002). Overall, thereis limited evidence on the effect of transport-related stress incircus animals (Anonymous 2004) but confinement inAnimal Welfare 2009, 18: 129-140

Time budgetsIn the wild, elephants (both species) spend anywherebetween 40 and 75% of their time feeding (Sukumar 2003).Asian elephants may consume between 33.6–44.4 kg ofgrass (1.5–1.9% of their bodyweight) in 12 h (Sukumar1992). African elephants can cover 30–50 km in a single day(Leuthold 1977) and African elephants spend 57% ofdaylight hours moving and feeding in the Okavango Delta(Evans 2006). In contrast, physical activity is limited in zoosand grazing is unavailable in 90% (18 out of 20) of Europeanzoos keeping Asian elephants (Taylor & Poole 1998).Circus animals, especially elephants, may be kept chained(shackled individually or picketed in lines) continuously for12–23 hours per day when not performing (Schmid 1995;Friend & Parker 1999). In four circuses, elephants spent12.6–22.7 hours per day shackled in an area 7–12 m2,although they could only move as far as the length of thechain, ie 1–2 m, 0.3–8.2 hours per day in a paddockmeasuring 22.7–72.0 m2and 0.3–2.1 hours per day trainingor performing (Schmid 1995). Thus, performing or trainingtypically occupy 1–9% of the day in circus animals (Schmid1995; Nevill & Friend 2006). Both shackling and picketingseverely restrict the degree of social contact amongst indi-viduals, basically reducing it to adjacent elephants (Schmid1995). However, many handlers claim that chaining isneeded, not only for safety reasons, but also because manytrainers regard it as a means of establishing and maintainingdominance (Schmid 1995; Friend & Parker 1999). Evenwhen not chained, circus elephants are housed in barrenpens surrounded by an electric fence which is viewed as a‘revolutionary’ improvement to the lives of circus elephants(Cimino 1994). In her study of 15 British circuses, Kiley-Worthington (1990) reported that half of the elephants wereallowed to move freely for one hour a day and that somespent the majority of the day in the electric-fenced pens. Ina study of elephant behaviour, trainers acknowledged thatpenned elephants were more relaxed and showed reducedstereotypic behaviour (Friend & Parker 1999). Whilst somedegree of socialisation is possible in penned elephants,uninhibited social interactions are not (Gruberet al2000).When animals are unsupervised, objects that might be usedby zoos as environmental enrichment (eg logs) are generallynot provided by circuses as they may be used to break thebarriers (Cimino 1994; Gruberet al2000).Kiley-Worthington (1990) noted that being shackled orconfined semi-permanently in beast wagons or stallsseverely restricted the behaviour of circus animals. Forinstance, there were times when carnivores did not haveaccess to exercise areas and would be kept in the beastwagons (which lacked furniture) all day except for perform-ances, or for periods of 10–12 h between arrival at a site inthe evening and the following day. Similarly, the ungulateswere often not taken out of their indoor enclosures for long� 2009 Universities Federation for Animal Welfare

StereotypiesIt has long been recognised that captivity may have delete-rious effects on an animal’s behavioural patterns. Normalbehaviour gives way to a higher percentage of inactivityand/or increased abnormal behaviour (self-directedbehaviour or self-injury) and stereotypies (Mason 1991a).Stereotypies are repetitive behaviours with no apparent aimthat develop when a captive animal is prevented fromexecuting a highly-motivated behaviour (Mason 1991a).For instance, stereotypic pacing in captive carnivoresgenerally increases during crepuscular hours (Weller &Bennett 2001) when wild carnivores are more active or,seasonally, when mate-seeking behaviour would beperformed in the wild (Carlstead & Seidensticker 1991).Although it is difficult to make generalisations about stereo-typies, they are commonly associated with a sub-optimalenvironment and poor or compromised welfare (Mason1991b). That is probably why primates confiscated fromtouring zoos and circuses exhibit undesirable behaviourmore than primates reared in recognised zoos (Mallapur &Choudhury 2003). Two studies examining transport in largefelids found very similar levels of stereotypic behaviour inboth zoo (22%) and circus (21.4%) animals (Nevill &Friend 2003; Dembiecet al2004), possibly indicating thatboth are sub-optimal environments. In addition, gatheringevidence suggests that stereotypies may also represent acaptivity-induced dysfunction of the central nervous system(Garner & Mason 2002; Masonet al2007).Stereotypic pacing varies widely amongst zoo carnivores,from an average of 0.16% of observations in red foxes(Vulpesvulpes)to 30% in lions (Pantheraleo)and 60% intigers (Bashawet al2003; Clubb & Mason 2007). A signif-icant proportion of this variation is explained by homerange and daily distance travelled: species that travel overlarge distances in the wild show higher levels of stereotypicpacing in captivity (Clubb & Mason 2003, 2007). Hand-rearing also negatively influences the development ofstereotypies. For instance, captive-bred, hand-reared bears,primates and African grey parrots (Psittacuserithacus)exhibit significantly more stereotypies than captive-bred,mother-reared individuals (Forthman & Bakeman 1992;Marriner & Drickamer 1994; Schmidet al2006) and thedevelopment of feather plucking and chewing in psittacinebirds has been linked to hand-rearing (Chitty 2003).Stereotypies tend to increase in frequency with increasingrestraint of movement and with more barren environments.For instance, circus elephants kept shackled or picketed,weave and head-nod more than in paddocks (Schmid 1995;Friend & Parker 1999), zoo bears and leopards (Pantherapardus)pace more in the smaller, off-exhibit enclosures thanin the larger, on-exhibit enclosures (Mallapur & Chellam2002; Montaudouin & Le Pape 2005), and captive parrotsperform more oral and locomotory stereotypies in barren

A review of wild animals in travelling circuses 135cages than in enriched cages (Meehanet al2004). Nevill andFriend (2006) found that access to an exercise pen for20–40 min had no effect on pacing in six circus tigers.However, tiger activity in the pen was inversely related topacing in the home cage, leading Nevill and Friend (2006) toconclude that access to an exercise pen is an importantenrichment and that it should be considered for longerperiods than 40 min. Some elephant handlers believe thatstereotypic behaviour has some beneficial effects. Forinstance, weaving stereotypies are said to aid circulation inthe same way that walking does in wild elephants (Friend1999). The frequency (percentage of all observations) ofstereotypic behaviour, however, is significantly greater(about 30%) in chained, circus elephants when compared toelephants in zoo or circus enclosures (about 4 and 10%,respectively [Clubb & Mason 2002]). There has been littlework on stereotypies in circuses, but evidence from Britainsuggests that all species of circus animal stereotype (Kiley-Worthington 1990). In both zoos and circuses, there wasevidence of prolonged distress and abnormal behaviour butthese were not any greater in circus animals than in zoo orother animal husbandry systems (Kiley-Worthington 1990).However, Kiley-Worthington (1990) did not consider pacing,bar chewing and pawing as stereotypies, although they arewidely regarded as such (eg Mason & Rushen 2006). Forfelids in circuses and zoos, larger crowds are related togreater frequency of pacing (Mallapur & Chellam 2002;Krawczelet al2005). As stereotypies normally indicate sub-optimal environments, a higher degree of stereotyping incircuses may be considered indicative of poorer welfare.common in circus as well as zoo elephants (Lindau 1970;West 2001), and more common in zoo than wild elephants(Schmidt 1986). Joint and hernia problems are thought toresult from circus elephants repeatedly assuming unnaturalpositions during performance (Lindau 1970; Kuntze 1989).In circuses, the lack of mud baths, which wild elephantstypically use for skin care, commonly causes severe skinproblems (Reitschel 2002). Other common health problemsin circus animals in Germany are tuberculosis, protein defi-ciency in primates and mange in camelids (Wiesner 1986).Cross-species transmission may be faster and morecommon in captivity than in the wild. For instance, Africanelephants may transmit the lethal elephant endotheliotropicherpes virus (EEHV) to Asian elephants in European zoos(Fickelet al2001). The two species do not meet in the wild.This virus is found in very young or stillborn calves, andrepresents a further threat (in addition to offspring infanti-cide and abandonment) to elephant reproductive success incaptivity (Fickelet al2001).Many non-domesticated animals are kept outside theirnatural geographic distribution and this may have negativeconsequences for their health. For instance, veterinarianstreating circus polar bears (Ursusmaritimus)performing inSpain, linked signs of depression and inappetance toextremely hot weather conditions (Bankset al1999) and, incolder and wetter climates, there is a greater incidence offoot infections in livestock (Vaarstet al1998).

Captivity-related stressRestricted physical activity and social interaction, incorrectfeeding practices or a forced reduction in the time spentforaging and in other highly-motivated behaviours, canrepresent stressors to non-domesticated animals. Stress canhave short-term behavioural and physiological effects, aswell as chronic, long-term, behavioural and physiologicaleffects (Hemsworth & Barnett 2000; Moberg 2000;Morgan & Tromborg 2007). It has been suggested that thegreatest stressor of captivity is the inability of captiveanimals to control the captive environment, ie the inabilityof confined individuals to escape or otherwise avoid thestressor (Sambrook & Buchanan-Smith 1997; Morgan &Tromborg 2007). The effects of even minor stressescombine to suppress immune function, reproduction,metabolism and behaviour (Moberg 2000).The circus environment seems likely to induce behaviouralproblems of the sort noted in other impoverished environ-ments with confined spaces, barren enclosures and socialisolation. Such effects vary from reduced reproductivebehaviour, exploratory behaviour and behaviouralcomplexity to increased abnormal, vigilance and hidingbehaviours, behavioural inhibition, aggression, fearfulnessand freezing behaviour (review in Morgan & Tromborg2007). Captivity-related stress is linked to the developmentof unusual diseases which affect captive-born and wild-caught but not wild, free-ranging cheetahs (Acinonyxjubatus;Terioet al2004). Given that social isolation,reduced space allowance and inappropriate housing condi-tions cause profound stress in domestic species (review inAnimal Welfare 2009, 18: 129-140

Diet and healthData on the diets of circus animals are scarce. Wiesner(1986) reported that protein deficiency is common in circusprimates. When zoo elephants are kept on a sand surface,they may eat sand and stones to the detriment of their health(Schulze 1986). Occasionally, circus keepers, ignorant ofplant toxicity, have fed inappropriate plants to elephants(Anderson 1968; Schaller 1983). Teeth problems (ie toothabnormalities) occur as a consequence of incorrect feedingpractices in captive elephants (Kurt & Hartl 1995) and wildungulates (Boyd 1986); Kurt (1995) has never observedteeth abnormalities in wild Asian elephants, although it isdifficult to examine wild elephants’ teeth. Some diseasesrarely encountered in the wild are present in captivity as aresult of bad feeding practices (Bankset al1999). Forinstance, circus lions developed botulism after consumingbroiler chickens (Greenwood 1985).The physical restrictions of the captive environment haveadverse effects on captive animals’ health. Elephantslacking physical exercise in zoos and circuses can becomeobese which, in turn, leads to joint defects and damaged feetand leg ligaments (Kurt & Hartl 1995). In a survey of62 Asian and 5 African elephants from three circuses andfive zoos, veterinarians found a high incidence of rheuma-toid disorders and one of the authors observed chronicarthritis and lameness in captive elephants (Clarket al1980). The development of lameness and foot problems is

136 Iossaet alMorgan & Tromborg 2007) and, given that there is partialevidence of their effect on non-domesticated species aswell, the housing conditions of circus animals are likely tocause severe stress to non-domesticated animals, althoughno data are available to test this hypothesis. On the otherhand, as we show in the next section, captivity-inducedstress impairs reproduction in many species.reason for the low or absent reproductive performance ofelephants in circuses is the lack of bulls. The keeping ofbulls is normally avoided in circuses for fear of aggression(Kurt & Hartl 1995). Aggressive behaviour is mostpronounced in the period ofmusth;some handlers try tocontrol aggressive bulls by beating them in sensitive areassuch as the ears, eyes and penis, which is thought to causecircus bulls to refuse to breed (Kurt 1995; Kurt & Hartl1995). For instance, of eight bull elephants kept in westernEuropean zoos, but formerly living in circuses, two weremoved to zoos before the age of 15 (prior to sexualmaturity) and successfully bred whilst five of the remainingsix, which lived in circuses until after 15 years of age,refused to breed (Kurt 1995). Husbandry practices seem tobe responsible for the lower reproductive success ofelephants in European zoos and circuses when compared toAsian extensive keeping systems (Kurt 1995; Taylor &Poole 1998; Clubb & Mason 2002).In the wild, environmental factors, such as resource avail-ability, predation and climate, limit animal populationreproduction, growth and mortality. In captivity, these envi-ronmental effects are limited. Consequently, reduced ornon-existent reproductive lifespan (Mellen 1991; Kurt &Khyne U Mar 1996; Wielebnowskiet al2002), dysfunc-tional copulatory behaviour (ie failure to copulate), infanti-cide or abandonment of offspring due to social disruption orhand-rearing (King & Mellen 1994; Kurt & Khyne U Mar1996), high infant mortality (Clubb & Mason 2007) and/orreduced life expectancy, all represent the deleterious effectsof husbandry-related stress.

The effects of captivity-related stress on reproductionReproduction is not normally included in welfare assess-ments (but see Crane 2007). However, we discussbreeding in captivity because it shows that captivity-related stress in circus animals is sufficient to have animpact on reproductive success.Many species are very difficult to breed in captivity as aconsequence of the detrimental effects of the captive envi-ronment on an individual’s development, modulation ofstress and arousal, and on the modification of social inter-actions (Carlstead & Shepherdson 1994). Breeding failureof captive animals is common and its origin can almostinvariably be linked to certain unnatural aspects ofcaptivity (Lindburg & Fitch-Snyder 1994). Even if viableoffspring are produced, the abandonment of the offspringby the mother is common. As a consequence, hand-rearingwas a widespread practice in captive environments (Young2003). However, hand-reared individuals may fail todevelop normal social and reproductive behaviours anddevelop abnormal behaviours (King & Mellen 1994; Chitty2003; Young 2003), which is the reason BIAZA-accreditedzoos only recommend hand-rearing for pre-determinedpopulation management purposes, eg according to TaxonAdvisory Group or European Endangered SpeciesProgramme recommendations (BIAZA 2005). It has beenrecommended that if hand-rearing is necessary in circuses,it should be accompanied by integration with conspecifics(Kiley-Worthington 1990). Hand-rearing and a lack ofsocial interactions are the main cause of breeding failure incaptive primates (King & Mellen 1994).Elephants are very difficult to breed in captivity for severalreasons, all of which are linked to environmental effects thatare more acute in circuses than in zoos. Elephants are highlysocial and, in the wild, live in matriarchal societies wheremothering skills are learnt through social experience (Kurt1995; Kurt & Hartl 1995). In captivity, in contrast,elephants are moved between establishments, therebydisrupting existing social bonds amongst group members(Datheet al1992; Lawset al2007) and thwarting the acqui-sition of mothering skills. Such treatment of females isthought to lead to the death of infants (Kurt 1995), and to bethe cause of higher percentages of stillbirths and infantmortality, due to infanticide, in European zoos and circusescompared to the wild (Kurt & Khyne U Mar 1996; Taylor &Poole 1998). To prevent infanticide, females giving birthmay be chained separately from the group (Schmid 1998).Stillbirths seem to have a correlation with an overweightmother and/or calf, and allowing female elephants moremovement or changing feeding practices would decreasefemale obesity (Kurt & Khyne U Mar 1996). Another� 2009 Universities Federation for Animal Welfare

Conclusions and animal welfare implicationsThis is the first study to review the welfare of non-domesti-cated animals in circuses and their suitability to a circus life.Information on circus animals is scarce, even to the extentthat the origin of most circus animals and precise numberskept, are unknown. In the UK, most animals appear to havebeen bred in captivity (Kiley-Worthington 1990) as opposedto being wild-caught, but this does not mean such animalsare fundamentally different from free-living animals. Weargue that there is no evidence to suggest that the naturalneeds of non-domesticated animals can be met through theliving conditions and husbandry offered by circuses.Neither natural environment nor much natural behaviourcan be recreated in circuses. Complex captive environments(naturalistic displays with plants, objects, perches, etc),such as those set up in good zoos can, in part, alleviatebehavioural problems stemming from captivity and providethe animal with a diverse array of stimuli (Carlstead &Shepherdson 2000; Masonet al2007). However, due totheir mobile life, circuses have a limited ability to set upcomplex environments and a non-domesticated animal’s lifeis consequently impoverished.Captivity can induce poor welfare in non-domesticatedanimals but circuses, in particular, fail to provide some oftheir most basic social, spatial and feeding requirements.The ability to execute many natural behaviours is severelyreduced, with partial evidence of a concomitant reduction in

A review of wild animals in travelling circuses 137welfare, health and reproduction, at least in the most well-studied species, such as African and Asian elephants. Inmany respects, and despite the lack of predation, foodshortage and adverse environmental conditions, animalskept in captivity experience poorer welfare than animals ofthe same species living free (eg cheetahs, Terioet al2004).Whilst it may be argued that hand-rearing, training andperformance in circuses may be suitable compensation for amore natural habitat and lifestyle (Hediger 1955), such asare found in the wild and in good zoos, this hypothesis hasnot been tested. Given that circus animals spent only 1–9%of the day performing or in training, we do not think thiswould be the case. We found no data to suggest that trainingor performance of circus acts is enriching or harmful. Incontrast, we found that human crowds are likely to causestress to non-domesticated animals.In Europe, the financial difficulties seen in the majority ofsmall circuses (Fleming 1994; Galhardo 2005) enhance therisk of poor husbandry, veterinary care and feeding for theanimals (Goldhorn & Kraft 1985). It must also be noted thatmost research on circus animals is conducted in the largestand better-financed circuses (eg Friend & Parker 1999;Gruberet al2000; Nevill & Friend 2003) and, therefore, islikely to represent the best husbandry and welfare incircuses rather than representing a cross-section of condi-tions found in circuses with a range of finances. Thus, thedata presented here are likely to be biased towards the bestcircuses, and are not representative of the norm.Price (1984, 1999) argued that species differ in their degreeof pre-adaptation to domestication and, for those speciesthat have not been domesticated, the captive environmentdoes not allow the expression of species-specific behav-iours compatible with husbandry techniques. Circuses maybe suitable environments for animals with low spacerequirements, simple social structures, low cognitivefunction, non-specialist ecological requirements and whichare capable of being transported without adverse welfareeffects, or animals habituated to human presence, such asdomesticated animals. In contrast, highly social, non-domesticated animals, such as elephants and wide-rangingcarnivores, which are amongst the most popular specieskept in circuses (Galhardo 2005), appear to be the leastsuitable to captive environments such as zoos (Rees 2003;Clubb & Mason 2007) and even less so to circuses(Amboseli Elephant Research Project 2007). This hasalready been recognised in many countries across the worldwhere all animals, or wild-caught animals, or some or allspecies of non-domesticated animals, are prohibited incircuses (eg Austria, Belgium, Costa Rica, Croatia, CzechRepublic, Denmark, Estonia, Finland, India, Israel, Poland,Singapore and Sweden). In the period from 1990–2005, thenumber of non-domesticated animals in British circuseshas been declining, possibly as an effect of the outbreak offoot and mouth disease in 2000–2001. We could not findreliable trend data on the number of circuses usingperforming animals but circuses with only humanperformers have grown in popularity in recent years. Thedeleterious effects that circus life has on individual animalsare of primary welfare concern. Circus animals spend themajority of the day confined, a small amount of timeperforming/training, and the remaining time in exercisepens. Circus cages/exercise pens and beast wagons were,on average, only 26 and 27%, respectively of the recom-mended size of zoo outdoor and indoor enclosures.Circuses, by their very nature, have a limited ability toimprove these conditions. Concerns have been raised aboutkeeping non-domesticated animals in circuses and thisreview has found that, although data are scarce, suchassumptions are, in part, supported. This warrants, at thevery least, further physiological and behavioural studies onthe effects of captivity and transportation, reproductivesuccess and the effects of training and performance, toimprove our welfare assessment of circus animals. Datacollated from other studies suggest that species commonlykept in circuses appear the least suited to a circus life.

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