Happy animals make good science

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<ul><li><p> http://lan.sagepub.com/Laboratory Animals</p><p> http://lan.sagepub.com/content/31/2/116The online version of this article can be found at:</p><p>DOI: 10.1258/002367797780600198 1997 31: 116Lab Anim</p><p>Trevor PooleHappy animals make good science</p><p>Published by:</p><p> http://www.sagepublications.com</p><p>On behalf of: </p><p> Laboratory Animals LtdLaboratory Animals Ltd</p><p> can be found at:Laboratory AnimalsAdditional services and information for </p><p> http://lan.sagepub.com/cgi/alertsEmail Alerts: </p><p> http://lan.sagepub.com/subscriptionsSubscriptions: </p><p> http://www.sagepub.com/journalsReprints.navReprints: </p><p> http://www.sagepub.com/journalsPermissions.navPermissions: </p><p> What is This? </p><p>- Apr 1, 1997Version of Record &gt;&gt; </p><p> at Universitats-Landesbibliothek on March 13, 2014lan.sagepub.comDownloaded from at Universitats-Landesbibliothek on March 13, 2014lan.sagepub.comDownloaded from </p></li><li><p>Happy animals make good science</p><p>Trevor PooleUniversities Federation for Animal Welfare, 8 Hamilton Close, Potters Bar, Hertfordshire EN6 3QD, UK</p><p>SummaryIn this paper the question is posed whether it is not only better for the animal to be happy, butwhether its state of mind may also have the potential to influence the scientific resultsderived from it. To ensure good science, the animal should have a normal physiology andbehaviour, apart from specific adverse effects under investigation. There is a growing body ofevidence from a wide variety of sources to show that animals whose well-being iscompromised are often physiologically and immunologically abnormal and that experimentsusing them may reach unreliable conclusions. On scientific, as well as ethical grounds,therefore, the psychological well-being of laboratory animals should be an important concernfor veterinarians, animal technicians and scientists.</p><p>Keywords Well-being; laboratory animals; endocrine; immune response; handling;experimental method</p><p>What are happy animals?Most people who have worked closely withanimals or who keep them as pets are awareif they are suffering or unwell; the signs maybe small but we become aware that all is notwell. Colloquially, we will say to ourcolleagues 'that animal is not happy'. Thesigns which tell us that there is somethingwrong are changes in the behaviour whichwe have come to expect from the individual,for example, we may find it sitting huddledin a comer, failing to greet us or lackinginterest in events taking place around it. Ifthe behavioural change persists, we takeaction and may even call in veterinaryadvice.Happiness and unhappiness, or distress,</p><p>refer to states of mind of the animal; theycannot be measured directly but the wholeconcept of animal welfare is based on thebelief that higher animals, like us, are able toexperience pain and pleasure. The best wayto decide whether an animal is happy ordistressed is by observing its behaviour. On</p><p>Corespondence to: Trevor Poole</p><p>Accepted 6 September 1996</p><p>this basis, I will define a 'happy animal' asone which is alert and busy (shows a widerepertoire of behaviour), is able to rest in arelaxed manner, is confident (outward goingand does not display fear towards trivial non-threatening stimuli) and does not showabnormal behaviour. It is, of course, impor-tant to be familiar with the particular.animal's character to make these judge-ments. Some individuals are naturallyextrovert and active, while others are quietand lethargic. In the laboratory, those of uswho care for animals like to think that ourcharges are happy and that any procedureswhich have to be performed on them causethem the absolute minimum of distress.In this article the question is posed</p><p>whether it is not only better for the animal tobe happy, but whether its state of mind mayalso have the potential to influence thescientific results which are derived from it.The most obvious cases of unhappiness willoccur when animals are sick or injured andsymptoms will vary from mild to severe.Generally, with modem laboratory practicethis source of distress has virtually beeneliminated. We take it for granted that</p><p>LaboratoryAnimals (1997) 31,116-124</p><p> at Universitats-Landesbibliothek on March 13, 2014lan.sagepub.comDownloaded from </p></li><li><p>Happy animals make good science</p><p>scientists do not work with animals whichare ill or injured. Nor do laboratory animalslack essential physical needs, such as food,water or suitable climatic conditions. Thereremain, however, a variety of potentialcauses of distress, such as social problemswith aggressive cage mates, overcrowding, orsocial isolation. There are also features of thephysical environment, such as loud orsudden noises, including ultrasound whichcan be perceived by rodents, dogs and smallerprimates, which might also be sources ofdistress. Finally, there are the attitudes andsometimes inexpert manipulations by staff.Mammals, particularly become distressed ifthey are badly handled, especially when theyare restrained by personnel unfamiliar tothem. This may be a common occurrence, asthe experimenter is not usually the personin day-to-day care. A factor which isincreasingly being recognized as a sourceof unhappiness, is the failure of the captiveenvironment to meet the animal'sbehavioural needs and assure its psycho-logical well-being. It is becoming apparentthat captive mammals can be bored or resortto abnormal behflviour if their environmentis not sufficiently complex and interesting tothem (Wemelsfelder 1990, Poole 1988).</p><p>What is good science?The quality of experimental laboratory ani-mal science depends on three essentialconditions being satisfied. Firstly, thereshould be an important problem for which ananswer is sought, secondly, the experimentshould yield unambiguous results whichprovide an answer to the problem and,finally, variables which are not under in-vestigation should be strictly controlled. Ishall take for granted the assumption that thefirst two conditions have been met and onlybe concerned with the third which, can alsohave a direct bearing on the well-being of theanimals. Good laboratory animal science isbased on normal, healthy subjects, unless theillness is itself the subject of investigation.Scientific method assumes the absence ofconfounding factors or uncontrolled vari-ables. Clearly, unhappiness might be aconfounding variable unless, for example, its</p><p>117</p><p>alleviation was the subject of the study, as inthe case of testing an anti-depressant. What-ever the subject under investigation, allunnecessary stress should be minimizedduring the experiment to reduce the varia-bility of the results and thus the number ofanimals required. This requires, firstly, athorough understanding of the animal and itsbiology and, secondly, experiments which arewell designed, statistically valid and appro-priate. Even in situations where the experi-ment itself creates unhappiness for theanimal, such as premature removal of young,any effect may be diminished or even lost ifthe animal was not happy in the firstinstance. We can therefore conclude that, inall aspects, apart from unavoidable adverseeffects of the experiment, the animal shouldbe happy.Most scientists working with animals will</p><p>make the assumptions that they will havenormal blood pressure, heart rates, levels ofstress hormones, immunological compe-tence, digestion, appetite and behaviour. Toavoid confounding variables, experimentalanimals should have both normal physiologyand behaviour. Some might argue thatbehaviour is of less significance than phy-siology, but this is based on the erroneoussupposition that mind and body are separateentities and that one will not influence theother. Recent scientific work has shown howthe brain, behaviour, hormones and even theimmune system, are all interdependent andthat disturbances in one of these systemscommonly influences one or all of the others(see review article by Martin 1989 and Bohus&amp; Koolhaas 1991).In fact, behaviouralchanges are usually more sensitive indicatorsof distress than physiological ones. I shallnow consider some of the main factors whichmay influence the psychological well-beingof laboratory animals.</p><p>Factors influencing psychologicalwell-being</p><p>Social factorsLaboratory mice are commonly kept in singlesex groups in stock cages. While femalesgenerally tolerate such conditions, males</p><p> at Universitats-Landesbibliothek on March 13, 2014lan.sagepub.comDownloaded from </p></li><li><p>118</p><p>fight and establish a hierarchy, but the typeof social structure depends on the number ofindividuals in the cage. Poole and Morgan(1973) found that, in small colonies of 3--4male CFW mice, the dominant's aggressionwas directed to few rivals and these sub-ordinates were highly intimidated and re-stricted in their movements about the cage.Five male mice however formed a linearhierarchy with each individual knowing itsplace and thus subordinates were able todevelop strategies to avoid conflict. In largercolonies of nine or more individuals thedominant was unable to control such a largenumber of subordinates, so that the socialstructure broke down after 3-5 days andanother dominant arose. This contrastedwith the situation in smaller groups of up tofive in number where, barring disturbance,aggression gradually decreased and wasminimal after 12-15 days. Physiological datafrom laboratory mice have shown that, instandard housing, subordinates exhibit high-er levels of stress and sex hormones thandominants (Hucklebridge et al. 1976, Bentonet al. 1978). In addition to experiencing fear,suffering injury and high levels of stresshormones, Beden and Brain (1984, 1985)found that the immunological response to anantigen (sheep red blood cell) was reduced insubordinate or defeated mice. Brayton andBrain (1973) found that crowding micelowered their resistance to a digenean para-site and Edwards and Dean (1977) alsoshowed that crowding affects the mouse'simmune response.Age is another important consideration</p><p>when housing male micej litter mates, unlesssignificantly disturbed will usually liveamicably together, as will members ofdifferent litters who have been groupedtogether from an early age. Clearly, whereverpossible, animals, should be kept in condi-tions where their social grouping leads to theminimum of aggression, and hence distress.There has been a tendency to believe that</p><p>isolation in the form of single housing isdistressing for other mammals, as it is forhumans. However, it has been found thatisolated male mice have hormonal profilessimilar to dominants (Brain 1975, Huckle-bridge et al. 1976, Brain &amp; Benton 1977,</p><p>Poole</p><p>Benton et al. 1978, Brain 1990), so thatsingly-housed mice do not suffer from 'iso-lation stress'. This finding is compatible withthe fact that mice are territorial in the wildand thus actively repel other males. How-ever, providing a simulation of the wild inthe laboratory may actually be deleteriousbecause Bishop and Chevins (1988) foundthat territorial male mice placed in an arenahad high levels of stress hormones, presum-ably associated with the defence of theirterritories. While access to social compa-nions benefits many species of laboratoryanimals, some solitary species, may have tobe kept alone because of their aggressivetendencies, for example, male rabbits andferretsj this is particularly common in caseswhere males have bred or been exposed tomembers of the opposite sex, or females haveinfant young. Even individuals of socialspecies must have adequate space to avoidone another and thus minimize any conflict.Bohus and Koolhaas (1991) reviewed the</p><p>literature on psycho-immunology and cameto the conclusion that social stress is onlylikely to impair immune function signifi-cantly when the animal is unable to exertsome control over the situation by develop-ing a coping strategy. Inability to escape froman attacker and chronic overcrowding areclear examples of situations which animalsare unable to control.It is important to remember that a rat is</p><p>not simply a scaled-up mouse. Rats are muchmore sociable than mice and consequentlyseem likely to suffer more when isolated,although Brain and Benton (1979) could findno evidence of isolation stress in this species.However, young rats show very active socialplay which involves both chasing and wrest-ling (Poole &amp; Fish 1975, 1976), so they needadequate space to do this. During theirdevelopmental stage, rats acquire skills andexperience; adult rats reared in deprivedconditions are not only less intelligent, butalso have smaller brains than those from richand stimulating environments (Renner &amp;Rosenzweig 1978). They are thus less normal,but this does not necessarily mean that theyare less happy.Beynen (19921 reviewed literature which</p><p>indicated that control rats in the same room</p><p> at Universitats-Landesbibliothek on March 13, 2014lan.sagepub.comDownloaded from </p></li><li><p>Happy animals make good science</p><p>as the experimentals showed raised levels ofcorticosteroids, as compared to controls inanother room. This suggests that some rats(and therefore possibly other animals) may beable to communicate their feelings to otherindividuals either by vocalizations or pher-omones and that situations which causedistress may also upset others within therange of these forms of communication.Mendoza et a1. (1991)found that squirrel</p><p>monkeys showed differences in levels ofcorticosteroids which related to their sex andsocial grouping. Females showed higherlevels when kept singly, with a single femalecompanion, or with a male. Three femaleshoused together appeared to be the minimumsocial group which would reduce the levels ofcorticosteroids to a normallevelj this num-ber also showed much higher levels ofreproductive cycling as compared to thesmaller groups or females paired with a male.Likewise male squirrel monkeys showedlower levels of corticosteroids when housedwith male companions. The practical im-plication for husbandry and breeding is thatthe minimum breeding group should consistof two males and three females.Both mammals and some birds have a</p><p>period of life when they acquire knowledgeof the world and are able to test its proper-ties while protected by a vigilant mother orfamily group. The developmental environ-ment determines, to a large extent the kindof situations with which they are able tocope when they reach adulthood. Duringchildhood they practise skills and motorcoordinations which will be of benefit inlater life. Many mammals play fight whenyoung and thus practise the strategies ofattack and defence which they will needwhen faced with real rivals. They showextraordinary curiosity and inventivenessand thus learn the properties of objects andother organisms in their environment.Mammals enjoy play and experimentation inthe sense that it is self-rewarding, so thatthey should be provided with a stimulatingand complex developmental environment.Likewise, the presence of a mother isimportant because it allows the young toexpress their wide repertoire of play andcuriosity without fear.</p><p>119</p><p>Early weaning is undoubtedly stressful formammals because of the upset caused bylosing their mothers. The problem is furtherexacerbated by the sudden loss of maternalantibody....</p></li></ul>