Evolution and Animal Welfare Author(s): Marian Stamp Dawkins Source: The Quarterly Review of Biology, Vol. 73, No. 3 (Sep., 1998), pp. 305-328 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/3036918 . Accessed: 19/07/2013 06:03

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This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions VOLUME 73, No. 3 THE QUARTERLY REVIEW OF BIOLOGY SEPTEMBER 1998

EVOLUTION AND ANIMAL WELFARE

MARIAN STAMP DAWKINS

Departmentof Zoology, Universityof Oxford Oxford,OX] 3PS United Kingdom E-MAIL: [email protected]

ABSTRACT Animalwelfare is a tbpicoften thought to reside outside mainstream biology. The complexity of themethods used to assess welfare (such as health,physiology, immunological state, and behavior) requirean understandingof a widerange of biological phenomena. Furthermore, the "welfare" of an animal providesa frameworkin whicha diversityof its responsescan be understoodas fitness-enhancingmechanisms.Different methodsfor assessing animal welfare are discussed, with particularemphasis on therole of an animal's own choicesand reinforcementmechanisms. No part of biologyis as yetable to explain consciousness,but byconfronting the possibility that nonhumananimals have conscious experiences ofsuffering, animal welfare studiesfarce a consid- erationof even thishardest problem of all biologicalphenomena in a particularlydirect and evolutionaryway.

INTRODUCTION change forbetter or forworse in the future.I shall argue thatmany of the so-called "indica- HOW CANTHERE be a scientificstudy of tors"of welfare that have been put forwardare animal welfare?If "welfare"just means best seen as evolutionaryadaptations, either "health,"then isn't animal welfaresimply vet- enabling the animal to counteract a threatto erinaryscience or animal health studiesunder itshealth and fitnessor, in the unnatural envi- anothet name? And ifanimal welfaregoes be- ronments in which humans often keep ani- yond thisand triesto take on mental as well as mals, showingthat the animal has failed in its physicalsuffering, how can it be more than an attemptsto do so. An action or physiological unscientific collection of assumptions-im- response that is effectivein the wild may possible to test-about what animals mightor become pathological and counterproductive mightnot be feeling? withinthe confines of a cage. One of the rea- The intentof thisarticle is to show thatani- sons why so many problems have been en- mal welfare,far from being a fringe activity countered in the studyof "welfare,""stress,;, outside mainstreambiology, could potentially "suffering"and related concepts is because an- be at the heart of biological thinkingabout imal welfarestudies have generallylacked the fitness-enhancingmechanisms in a varietyof evolutionaryframework that characterizesso disciplines. Assuming that "welfare"includes much else in biology.Animal welfare,in other not onlycurrent health statusbut also a variety words, needs a dose of Darwinian medicine of behavioral,physiological and immunologi- (Nesse and Williams 1995). cal indications that health status is likely to Before thistreatment can be administered,

The QuarterlyReview of Biology, September 1998, Vol. 73, No. 3 Copyright? 1998 by The Universityof Chicago. All rightsreserved. 0033-5770/98/7303-0002$2.00

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This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions 306 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 however, it is necessary to distinguishthree their plants in the way that dog owners care typesof questions that are oftenraised about about thatof theirpets, but it is the belief that animal welfare,but are almost equally often animals have something extra-a mental ca- confused. The firstone is,what objective mea- pacityfor experiencing pain, thirst,boredom surements-biochemical, physiological, be- and other mental states-that gives animal havioral-should we use to evaluate whether welfare its moral edge (Duncan 1993). This the welfareof an animal is poor or good. As argumentis also reflectedin the scientificlit- discussed below,biochemistry, physiology and erature, where it has been held that "suffer- behavior are all respectable scientificdisci- ing" includes mental suffering(Dawkins 1990; plines, and there is no real problem about us- Webster 1994), and even that sufferingdoes ing them in animal welfarestudies. Their use not occur unless there is a conscious experi- might be controversialand their interpreta- ence (Duncan 1993, 1996; Duncan and Peth- tion may be subject to doubt in some circum- erick 1991). stances,but theirscientific credentials are not. Animal welfare is thus left with a serious The second type of question is, however, problem. If it sticksto what is scientificallyob- more difficult.Are animals thatcan be shown servable, it leaves out what distinguishesfor to have these objectivelymeasured symptoms many people the studyof "welfare"from the consciouslyexperiencing what humans would studyof physical health, namely, conscious ex- call suffering,if we were experiencing these periences of sufferingand well-being.On the same symptoms?For example, ifa nonhuman other hand, ifit accepts thatconscious experi- animal showsclinical signs of exhaustion, and ences (such as those humans call fear, pain these are comparable to those thatgive rise to and frustration)are also sensed by other spe- veryunpleasant experiences in humans, are cies, it runs headlong into the problem of we justified in concluding that the animal is studyingconscious experiences that no field also suffering?This kind of question poses of science, despite many attempts, has yet more problems than the firstone because it come to gripswith. touches on the greatestremaining mysteryin The thirdtype of question thatcan be asked biology-that of conscious experience. Deter- about animal welfare arises out of a concern miningif an organismis conscious or not raises for animal suffering,but is logically distinct difficultiesof a differentorder of magnitude from the issue of whether animals suffer from finding out whether a particular treat- (Stafleu et al. 1996; Fraser et al. 1997). Is it ment resultsin a raised hormone level, forin- ethicallyright or wrongto treatanimals in cer- stance. Despite the avalanche of books that tain ways? Tannenbaum (1991) argued that has recentlyappeared on the subject of con- scientificstudies of animal welfarecan never sciousness (e.g., Dennett 1991; Edelman 1992; be undertakenseparately from an ethicalframe- Crick 1994; Penrose 1994; Weiskrantz1997), work. Rollin (1995) even argues that it is a we have not achieved the same level of un- waste of time to ask whetheran animal is suf- derstanding about consciousness as we have fering,and the onlyjustifiableapproach is al- (throughobjective measurements) about hor- waysto worktoward reducing suffering."Ani- mones and behavior. Insofaras it concerns it- mal welfare" is thereforeput into the same selfwith conscious experiences of sufferingin category as "public health": it is assumed to animals, the studyof animal welfarecould be be a goal toward which everyone should be accused of strayingoff the straightand narrow working.The viewI shall take here is thatmix- path of what is strictlyscientific. ing ethical questions about how animals ought Yet, when people express a concern about to be treatedwith factual questions about wel- animal welfare,it is preciselythe conscious ex- fare is likely to lead to confusion, since hu- perience of sufferingthat worries them most. mans do not automaticallyknow what condi- Animal welfare has a higher moral profile tions are best for the welfareof animals. Facts than, say,plant welfare,because more people alone, without preconceived moral views, believe that animals consciously sufferthan could lead humans to take a differentview of believe thatplants do. Orchid growersmay be how animals ought to be treated (Dawkins concerned about the health and growth of 1980). In any case, the general viewthat scien-

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions SEPTEMBER 1998 EVOLUTION AND ANIMAL WELFARE 307 tificand ethical questions (what "is" and what persistent tendency to believe that a good "ought to be") are differentand should not be measure of welfare(with multiple attributes if confused, has much to be said for it (Broom necessary) is attainable ifwe onlyknew how to andJohnson 1993). constructit. In thissection, I shall firstreview I propose, therefore,to keep these three the main component measures of animal wel- typesof questions-the symptomsof good and fare thatare currentlyin use. I will emphasize poor welfare,the conscious experience of suf- the strengthsand weaknesses of each, as well fering,and our ethical attitudes toward ani- as the importance of taking a broad view of mals-in their own reasonably watertight whatconstitutes good welfare.I shallthen argue, compartments.Here I shall concentrate on however,that the goal of animal welfarestud- the firstquestion, bydescribing the various in- ies should not be to put thevarious constituent dicators and symptomsof animal welfarethat partsinto a single measure, or to assignvarious are now in use, and how theyshould be seen values to differentmeasures and thenadd them in an evolutionarycontext. I shall then briefly up to arriveat a total welfarescore. Rather, I examine the connection between whatwe can shall argue that many of the so-called symp- observe and what perhaps can infer about toms of poor welfareare in fact evolutionary conscious experiences in other species. The adaptations,that is, defensesagainst threats to moral implications of welfare studies I shall fitness.Some defenses (such as pain and fear) leave firmlyalone, allowing readers to decide are "unpleasantby design" (Nesse and Williams for themselveswhat theyshould do with the 1995:26) in the sense thatthey temporarily re- factsthat are now available. duce well-being but enhance health and re- production in the long term.Such a viewpoint MEASURING WELFARE IN ANIMALS has a profound effecton what we should con- The twobig challenges in the measurement clude about the welfareof an animal. of animal welfarehave been to define what is meant bywelfare, and to decide how to mea- GOOD AND POOR WELFARE sure it (e.g., Dawkins 1980; Curtis 1987; Gon- Injury,disease and death are the obvious you 1993; Mason and Mendl 1993; Moberg veterinarysymptoms of poor welfare.A wide- 1993). In fact,the pursuitof "measures ofwel- spread consensus both within and outside fare" has become something of a Holy Grail. biology is that good welfare,at the veryleast, As Fraser (1995) has pointed out, however, means that animals are free fromdebilitating many of the difficultiesin definingand mea- diseases, injury and malnutrition,and that suringwelfare have arisen because ofmistaken theyare not kept in conditions thatlead to the notions about the "welfare"concept. It is not development of physicaldeformities (Wolfen- a simple variable, like the height of building, sohn and Lloyd 1994; Fraser 1995). Some- that can be easilymeasured in metersor feet. times the firstsigns of poor welfare are de- On the contrary,it is a complex attribute, tected intuitivelyby a pet owner or a livestock more like the "safety"of a building ratherthan owner, or can be assessed quantitativelyby itsheight.Just as we do not expect to be able to looking at such indicators as posture, body measure thesafety of a building bysome single weight,or whetherthe eyes are open (Morton quantitativeexpression thatwill be valid in all and Griffiths1985). At other times,injuries or respects and under all circumstances,so we deformitiesmay be apparent onlyafter death, should not expect to arrive at a measure of as withbone breakages (Gregoryand Wilkins welfareexcept as a traithaving multiple attri- 1989) or some skeletal asymmetries(M0ller butes and being differentunder various cir- et al. 1995). There are often good practical cumstances. reasons formaking sure thatsymptoms of dis- While it is now generallyrecognized thatno ease and injuryare alleviated or avoided: ani- single measure of welfare is adequate on its mals kept in conditionswhere theyare subject own (Dawkins 1980; Mason and Mendl 1993), to infectionsor injuriesare more likelyto die, there is still disagreement on how different and thusfail to produce the meat, eggs or milk measures should be put together and which that are commerciallyvaluable. But it should ones should be given priority,and there is a not be assumed thatcommercial pressures will

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions 308 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 always lead to the avoidance of even these mals have evolved; it comes into play before a gross measures of poor welfare.The produc- physicalinjury happens. In fact,by causing an tivityof a farm that produces eggs may be animal to flee or hide, fear probably evolved greater if birds are kept under conditions in and reduced the likelihood of physicalinjury which some of them were injured ratherthan occurring at all. Just as pain helps to avoid if conditions were improved (at some consid- death, fear helps to avoid pain. Natural selec- erable expense) so that injury rates were tion has led to mechanisms that operate ear- lower. Such grosswelfare measures should be lier and earlier,long before health and fitness made at the level of the individualanimal, not are actuallythreatened. Thus theseunpleasant- the farm unit. We should not assume that a by-design,death-avoiding mechanisms come productive farm is one where the welfare of into play notjust when death is imminent,but animals is guaranteed. sometimeslong beforedeath is likelyto occur. Disease, injuryand other clinical signsof ill- In other words, there may be preclinical or health are indicators of poor welfarefor two subclinical changes in response to a potential reasons. First, they show that the animal is threat,even when the health of the animal is more likelyto die. Second, theyindicate that apparentlygood. It is thereforeimportant to theanimal's owndefense mechanisms may have consider other measures of welfarebesides the been activated,and thesemay be extremelyun- obvious ones of overtdisease and injury,even pleasant in theirown right.For example, it is thoughthese are generallyconsidered to be the now widely accepted that pain serves a num- cornerstoneof all good welfareassessment. ber of important functions including the avoidance of dangerous situationsand simply BEHAVING "NATURALLY keeping damaged limbs immobile while they Over 30 yearsago, Thorpe (1965, 1969) ar- heal (Wall 1979; Bateson 1991). This means gued that the abilityto performnatural pat- that an injured animal has reduced welfare ternsof behavior was an importantcriterion of both because its injury makes death more welfare.He believed that preventinganimals likely (through infectionand vulnerabilityto from carryingout their "natural instinctive predation) and also because itsadaptive mecha- urges" (1965:79) inevitablyled to poor wel- nismsfor dealing with injury (making death fare.For example, small bare cages thatdo not somewhatless likelyin the long term) include allow chickens to scratch,dustbathe or show highly unpleasant sensations of pain. Pain other behavior patterns that they normally evolvedbecause, bybeing unpleasant, it keeps would in "natural" systemswere, he argued, us away from the larger evolutionarydisaster inevitablydetrimental to welfare. of death. Pain is part of a mechanismfor help- The idea thatthe welfareof animals can be ing us to avoid immediatesources of injury,and judged by the extent to which they are able also to refrain from repeating actions that to performtheir natural behavior patternsis have resulted in damage. widespread (e.g., Kiley-Worthington1989). It This distinctionbetween poor welfaredue has become writteninto the legislationof vari- to injuryand disease perse, and poor welfare ous countries. For example, in Germany,the owing to the animal's own mechanisms for Animal Protection Act (1972) required that dealing withinjury and disease, has important anyone keeping an anitnalshould "provideac- implications for assessing the welfare of ani- commodation which takes into account its mals thatare freeof disease, uninjured and, in naturalbehavior." The U.K. FarmAnimal Wel- the opinion of a veterinarian,in good health. fare Council has stressed the importance of One viewis thatsuch animalsmust be in a state the "Five Freedoms," which include the free- ofvery good welfareindeed, and could not pos- dom to express normal behavior. The current siblybe suffering.The other view is that they enthusiasm for "environmentalenrichment" could be sufferingif their defense mechanisms programsin zoos (Markowitz1982; Carlstead for avoiding disease and injury had already 1996) restson the assumption that the more been activated. For example, although pain of its natural behavior patterns an animal is resultswhen an injuryoccurs, fear is also one allowed to show,the betterits welfare must be. of the injury-avoidingmechanisms that ani- Although humans may like to see animals

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions SEPTEMBER 1998 EVOLUTION AND ANIMAL WELFARE 309 behaving in naturalways, it is importantto ask than the wasp had dug herself,the wasp would whetherthe animal's welfareis genuinelyim- switchto diggingthe side tunnelmuch sooner. proved by such supposed enrichment.When In other words, it was the end result-in this we thinkcritically about thisissue, it becomes case a shaftof a certain length-that was im- clear thatthere is no necessaryconnection be- portant,not whetherthe wasp had performed tween the naturalness of behavior and good a certain amount of digging behavior. There welfare.For example, domestic and zoo ani- are othercases, however,such as nestbuilding mals show on average less escape and anti- in hens, where behavior seems to be much less predatorbehavior thanwild ones, but itwould controlled by endpoint and much more af- be incorrectto argue fromthis that the welfare fected by performance.Hughes et al. (1989) of captiveanimals thereforemust be lowerbe- gave hens either preformednests (previously cause of the "deprivation"of not havingto flee built by the same hen) or flat littersurfaces. frompredators (Dawkins 1980; Baxter 1983). Nest-buildingbehavior was not inhibitedby a If thiswere true, then environmentalenrich- nest alreadybuilt, and the hens went through ment programs should include a regimen of nest-buildingbehavior even though a nestwas frighteningthem by exposing them to their already present. Nest building thus seems to predators.On the otherhand, it could equally be an example of where the "behavior itselfis well be argued thatthe welfareof captive ani- a potentsource of reinforcingstimuli" (Herrn- mals is actuallybetter than that of their wild stein 1977). counterparts,since the protection offeredby Unfortunately,there are no general rules captivityand the domesticenvironment means for predictingwhether a given behavior pat- that theyare less likelyto experience fear,or ternper sewill be importantto the captive ani- injuries that might be sustained by escaping mal or rendered unnecessaryby providing the froma predator's attack.In order to settlethe rightenvironmental stimuli; therefore, there issue one wayor the other,we need more evi- is no way,without doing specificexperiments, dence. The naturalnessof an animal's behav- of inferringwhat the resultswill be in a captive ior is no guarantee of either good or bad wel- animal that does not demonstrate those be- fare.At most,a comparison of the behavior of haviors. In nature, functionalresults (such as a captive animal with that of its wild counter- replenishingfood reserves,building nests, find- parts can only alert us to the possibilitythat ingwater)can be achievedby a varietyof mecha- poor welfaremay resultfrom inability to per- nisms. If, in nature, a given species chases its formcertain behaviors. preyfor a long distance before eating it,there There is no simple link between "depriva- is no a prioriway of knowingwhether the ani- tion" of a natural behavior and welfare be- mal is motivatedto chase even when provided cause variousbehavior patternsare controlled withadequate food. Behavioralecologists have in differentways, which means that there will been much more concerned withfunctional be a varietyof resultswhen captiveanimals are considerations of what animals do and much preventedfrom performing behaviors seen in less concerned withthe mechanisms bywhich wild animals. There is an important distinc- they achieve them. We are in great need of tion between the two ways that behavior can a returnto the ethological balance of asking be brought to an endpoint. questions about both function and mecha- In some cases, a whole sequence of be- nism (Tinbergen 1963), as well as seeing the haviors can be terminated when an animal connections between them but realizing that achieves a particular goal or endpoint. For theyneed differentsorts of answers (Duncan example, female great golden digger wasps 1995). The actual mechanism by which a be- (Sphex ichneumoneus)dig burrows in which havioral sequence is controlled, and conse- theylay their eggs. Each burrow consistsof a quently the effectsof keeping an animal in main shaft (which the wasp digs first)with a conditionswhere it cannot performthe behav- lower side tunnel that branches off. Brock- ior, are only discoverable by empirical tests. mann (1980) showed that, if she artificially Only when we understand the mechanism of lengthened the main shaftin the earlystages control and the behavioral and physiological of construction so that it was much deeper consequences that resultfrom animals being

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions 310 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 prevented from carryingout such behavior Clutton-Brocket al. 1982), theymay also suffer will we be able to decide whether departures depression of their immune functionas a re- fromwhat is natural are good or bad for an sult of the high levels of testosterone(Gross- animal's welfare.This willprobably be a rather man 1985; McCruden and Stimson 1991). Fe- painstakingand in some waystedious task,as male junglefowl lose up to 17% of theirbody the same questions willhave to be asked about weightwhile incubating eggs. Normally,such differentspecies and about differentbehav- a weight loss would be viewed as a deteriora- iors withinthe same species. tion of physical health and a decline in wel- Such considerations of "deprivation" and fare.The birds,however, appear to have been welfare in nonhuman animals also apply to selected to be anorexic during this period, our own species of course. We live unnatural since theydo not eat even ifoffered food while lives in the sense that we fail to show many sittingon the nest (Sherryet al. 1980). formerbehaviors in whathas come to be called The factthat individual animals maychoose the "environmentof evolutionaryadaptedness" to sacrificetheir own welfare(asjudged bysus- or EEA (Nesse and Williams 1995). Some of ceptibilityto disease, injury,and failureto per- these "deprivations" (such as too little exer- form individuallyessential behavior such as cise) resultin poor welfare,whereas others (such feeding) means that longevityof the individ- as bettertemperature control in our environ- ual may not be the most reliable criterionof ments) have enhanced welfare.Taken alone, overallwelfare. This in turnmight suggest that the degree of unnaturalness in our lives is a the welfare of animals should be judged by poor guide to the assessmentof our own wel- theirreproductive success-a conclusion that fare.We need other criteriato help in thatde- would obviouslyfind favorwith farmerswho cision,both forourselves and forother species. seek high egg production or large littersof piglets-or theirfitness (Broom andJohnson LONGEVITY, REPRODUCTIVE SUCCESS 1993). But even this conclusion could be in AND FITNESS error.Selection does not necessarilyfavor maxi- mal reproductionor even reproductionat all, One solution thathas been proposed to the as is shown by the sterileworkers found in eu- problem of whetheran animal's welfareis ad- social insectsand naked mole rats (Jarviset al. verselyaffected by being unable to perform 1994) as well as delayed reproductionin many certainkinds of behavior is to measure itslon- bird species (e.g., Emlen and Wrege 1989). gevity.Hurnik (1993) has argued thatnot only Furthermore,while loss of fitnessmay be can longevitybe objectivelyquantified but it a useful measure in conservation,such as in is also a directreadout of an animal's welfare, judging adverse effectsof tourism on wildpop- since itwill be a measure of howwell itsvarious ulations (Hofer and East 1998), it could be been biological "needs" have satisfied.He ar- positivelymisleading in the more artificialen- gues that the more adequately its needs are vironment of a commercial farm. Here "fit- satisfied,the greaterits welfare and the longer ness,"as definedby reproductive success, could the animal may be expected to live. be the resultof selectivebreeding (or genetic The main problem with this approach is modification) that is quite incompatible with that,as Fraserand Broom (1990), Fraser(1995) good welfare. For example, a cockerel of a and others have pointed out, animals have broilerbreed mightsire a large number of off- been selected to reproduce, not just to live a springand thus be said to have higher fitness long time as individuals. A consequence of than a barnyard cock with a much smaller gene level selection is that the health, longev- number of survivingoffspring. It does not fol- ityand even survivalof individualanimals may low, however,that the broiler cock, kept per- be reduced in the interestsof gene propaga- manentlyon low lightand restrictedfood, was tion.Avery obvious example of thisis the con- in a betterstate of welfare,because the large siderable costs, including reduction in physi- number of offspringcould have been achieved cal health, that occur in animals during the despite its compromised health. In an ex- breeding season. Not onlydo male animals of- tremecase, an unhealthybird could have been ten sustainserious injuriesby fighting and loss strippedof sperm and itslarge number of off- of conditioning throughfailing to feed (e.g., spring attained by artificialinsemination.

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions SEPTEMBER 1998 EVOLUTION AND ANIMAL WELFARE 311

Once again, although we have a measure- cells and by inhibitingproduction of insulin. mentwe can use, additionalcriteria are needed As a consequence, the amount of plasma glu- before we can draw valid conclusions about cose is increased providingimmediately avail- welfare. One of the most widely used, most able energy. This energy helps prepare the quoted and most misunderstood are a suite body for fast and possibly prolonged action, ofphysiological variables collectively known as such as fightingor fleeing from a predator. "stress"symptoms. Selye (1956) called thiswhole set of symptoms the GAS or General Adaptation Syndrome, STRESS: PHYSIOLOGICAL SYMPTOMS and he believed that one of the verystriking OF POOR WELFARE things about it was that the reactions of the Even before overtsigns of disease, injuryor bodywere very similar when exposed to a wide physicaldeformity are noted, it may be possi- range of differentstimuli such as electric ble to detect internal signs of disturbance of shock, cold or injury.In Selye's view, "stres- metabolism that, if allowed to continue un- sors"were stimulithat could be demonstrated checked, mightlead to visible symptomsof ill to triggerthis syndrome. "Stress" symptoms, health that are generally agreed to indicate and in particular a rise in glucocorticoid lev- poor welfare (Moberg 1987). Animal welfare els, were thoughtto be a clear indication of a studieswould therebyhave the same objective wide range of unpleasant or aversive states, basis as veterinarymedicine, but with the and thus of great importance in the assess- added bonus that since it is concerned with ment of animal welfare (Barnett and Hems- subclinicalor preclinicalsigns of ill health,the worth 1990; Broom andJohnson 1993). welfare of even apparently healthy animals A number of serious conceptual and factual can be assessed. Two major problems remain problems, however,have subsequentlyarisen forsuch a "litmustest" of animal welfare:what thatcast doubt on the universalityof glucocor- physiological variables should be used, and ticoids as "stress" hormones and thus mea- what level of a given variable should corre- sures of poor welfare. The stressresponse to spond withsuffering or otherwisegive rise to differentso-called stressorsmay not be as simi- concern for the animal's welfare. lar as once thought, the apparent similarity The firstof these problems-the physiolog- resultingfrom a common reaction to being ical variables to look for-has largely been tested and handled (Dantzer and Mormede tackled by referringto a suite of so-called 1983; Moberg 1993; Rushen and De Passille "stress"symptoms. Unfortunately, there has 1992). Even more serious, higher glucocorti- been a great deal of confusionboth about the coid levels (as well as increased heart rate and meaning of stress and about the interpreta- other symptomsof stress) occur in situations tion of the variables that are supposed to re- that could be considered very pleasurable, flectits presence (Archer 1979; Rushen 1991; such as duringsexual behavior,feeding behav- Broom andJohnson 1993; Moberg 1993; Weip- ior or anticipation of food (Szechtman et al. kema and Koolhaas 1993; Sapolsky 1994; 1974; Colborn et al. 1991). Toates 1995). Originallythe termwas applied This generalityof the stress response ob- to the group of adaptive responses that many served in situationsregarded either as pleas- animals show when faced witha situation re- ant or as unpleasant has caused much con- quiring some sort of immediate action, such fusion. Despite many attempts to strip the as fleeingfrom a predatoror fightingoff a rival stress response of its negative connotations, (Cannon 1929). Some of these responses,such such as Selye givingone of his books the title as deeper breathingand increased heart rate, Stresswithout Distress (1974), the word stressin obviouslyprepare the animal for an action to popular usage continues to implysomething come by delivering oxygen more quickly to unpleasant, damaging and definitelyto be the tissues that need it. Others, particularly avoided ifat all possible. A more neutralword the activationof the HPA (hypothalamic-pitu- such as "arousal," "excitement"or "physiologi- itary-adrenocortical)system involve cortico- cal activation"would not bias an answerto the steroid hormones that affectthe metabolism question of whether a particular instance of of glucose, both bylowering its transportinto the GAS was positive or negative, but when

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corticosteroidsare labeled "stress"hormones, tions that the animal finds aversive (and will manyimmediately are led withoutthinking to attemptto avoid), thus givinga criticalrole to the conclusion that if some activitycauses a the animal's own response to the situation,a risein "stresshormones" itmust, by definition, point we will returnto later. be bad forthe animal's welfare.Indeed Broom The advantage of this viewpoint is that it (1991), in discussing elevated corticosteroid allows us to get around the realization that secretion in domestic animals that are han- highlypleasurable situationscan also give rise dled, argues that"a greaterresponse indicates to elevated corticosteroidlevels (a kiss is not poorer welfarethan a smaller response." stressful;the presence of a predator is). The Recently, even more confusion has crept disadvantage is thatthe word "stress"has now into the literature.The word "stress"has been become so widelyused in situationswhere no used to cover not onlyphysiological responses one has even looked for corticosteroids(such involvingincreased glucocorticoid secretion as in manycurrent studies on fluctuatingasym- but also anynegative effect whether it is medi- metry)that even this understanding may not ated through corticosteroidsor not. Thus, in be enough to stem the tide of confusion. Fur- a varietyof animals, it has now been shown thermore,an evolutionaryapproach to the way that symmetricalindividuals are more attrac- animals respond to potentiallydamaging situa- tiveas mates than ones thatare asymmetrical tions gives us yet another reason why"stress," (M0ller and Swaddle 1997). Symmetry,such even when restrictedto demonstrablyaversive as shown by the abilityto grow two horns or situationsin which there is known to be a rise twotail feathers of the same length,is believed in corticosteroidlevels, may not be the best to be an indicatorof mate qualitybecause sym- or most useful way to forge the link between metryis difficultto achieve in the face of per- physiologyand measures of poor welfare. turbationsin the environment(Parsons 1990). Even a very simplistic Darwinian starting Animalsthat have enough resourcesto achieve point would lead us to expect that animals symmetryare thus thought to be of higher would behave and respond physiologicallyin quality.Perturbations that can potentiallydis- adaptive ways in the face of threats to their rupt developmental processes are unfortu- survivaland reproduction.But it would be ex- natelyreferred to as "stressors,"even though tremelyimplausible to suggest that all such there maybe no evidence thatcorticosteroids threatswould be met in the same way.For ex- are involvedat all. ample, if an animal's life and well-beingare The inexorable (but misleading) logic being put at riskby dehydration, we would not about stressnow goes like this:Stress was origi- expect it to respond in the same way as if it nally defined as any factorwhich leads to in- were threatened by an approaching predator creased corticosteroidsecretion. In popular or to the danger resultingfrom having a bro- thinking,however, stress implies something ken limb. Seeking water,running away from a unpleasant and bad forwelfare.Therefore any predator, or remaining immobile to prevent increase in corticosteroidlevels must be bad furtherdamage to an injuryare all adaptive forwelfare and that in turnmust be stressful, responses,but it is clear thatthey are all differ- regardlessof whether it leads to increased cor- ent. Some animals respond to predator attack ticosteroidlevels. Put in thislight, it is easy to by fleeing,others by freezingand remaining see thatthe confusion about the word "stress" motionless. It is thereforenot surprisingto is considerable and is made up of several dif- find that the physiological responses that ac- ferentsources of error. company and give rise to these disparate be- The solution thatToates (1995) proposes is haviors would also be different (Freeman not to abandon the concept of stress alto- 1985). The fact that the physiological"stress" gether,but to refine the definitionin such a response occurs after such a wide varietyof way that elevated corticosteroidsbecomes a differentstimuli, such as injury,cold, and dis- necessary but not a sufficientcondition for ease, is quite remarkable. calling something a stressor.The extra ele- But the fact that some diverse stimuligive ment he proposes is that elevated corticoster- rise to a common "stress"syndrome does not oid levels should be shown to occur in condi- necessarilymean thatall threatsto survivalwill

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions SEPTEMBER 1998 EVOLUTION AND ANIMAL WELFARE 313 do so. We must go back to the considerations tivelyengaged in pleasurable situations.Ani- of why the "stress"response occurs at all. As mals seek out and move towardsfood, water, we have previouslyseen, stress prepares the mates or a comfortablenest, and theyuse the body for action by making it ready for "flight same limbs and muscles to achieve those goals or fight."It followsthat threatsto the animal as theydo to avoid threateningsituations, and that are not met most adaptivelyby intense theymay do so just as actively.It is therefore activitymight not be accompanied bya "stress" to be expected thatpositive reinforcement of response at all, yetcould stillbe highlyaversive sexual activitywill have symptoms,including to the animal. Indeed, we find some animals increased heart rate and raised corticosteroid thatrespond to predatorsby remaining immo- levels, similar to those induced by aversiveor bile do not show the "stress"response. They punishing stimuli. do not need the increased energythat gluco- Increased corticosteroidlevels are thus not corticoidsprovide and a pounding heartmight necessarily indicative of negative emotional actually make them less immobile and thus states or poor welfare,but of more general more in danger of being spotted (Gabrielsson states of excitement that can be either pleas- et al. 1977). ant or veryunpleasant indeed. The onlydiffer- A similarargument holds between different ence betweenstates we referto as good welfare threatsposed to the same animal. If the wel- and poor welfaremay be whetherthe animal fare of an animal is threatenedby a predator, activelyattempts to go toward or away from it maywell need to prepare foraction, but not something,that is, whether the animal findsa if its welfareis being compromised by a lack situation aversive or punishing. This in turn of stimulation.For this reason, simple com- may be reflected physiologicallyonly in mi- parisons between levels of corticosteroidhor- nute brain differencesbetween the twostates. mones in two situationscan be extremelyun- Agony and ecstasymay be similarexcept fora reliable guides to the welfare of animals. In small crucial differencethat may be verydiffi- layinghens, a comparison is sometimesmade cult to detect. What have been described as between caged birds and those kept in larger physiologicalmeasures of stresstend to be mea- groups or range freely.The threats to free- surementsof preparation for action, whereas range birds (predators,interactions with large what we really need to know is whether the groups of other birds), however,are quite dif- decision-making mechanisms of an animal ferentfrom those of caged birdswhere lack of have evaluated the situation as aversive or freedom to turnor the absence of nest boxes pleasurable. Until we have a betterdeveloped could be expected to give rise to a different physiologyof decision and choice in animals, set of physiologicaland behavioral responses. we will need to supplement our physiological Anysimple conclusion based onjust one phys- measures with behavioral measures of aver- iological stressvariable is thereforebound to sion (see next section on behavior and ani- be suspect. mal welfare). There is another evolutionaryreason why In addition to thisdifficulty of relyingonly we should expect "stresshormone" levels to on corticosteroids,there are other practical be an unreliable guide to welfare:There is a problems that have beset studies on "stress" greatdeal of overlap between physiologicalre- responses. Rushen (1991) documents a num- sponses to pleasurable and aversivesituations. ber of studies that actually describe com- Preparation for action is as characteristicof pletely contradictoryresults. Corticosteroid manypleasurable responses as it is of aversive levels in layinghens have been reported as be- ones. Both the prey that runs away from its ing higherin cages than in pens (Gibson et al. predator and the predator thatruns afterit in 1986), lower in cages than in pens (Koelke- anticipationof somethingto eat have to make beck et al. 1987), the same (Craig et al. 1986) or a major physical effortand to mobilize their dependent on the level of handling (Mench resources to do so. It is thereforenot surpris- et al. 1986). Since quite differentconclusions ing thatmany of the "stress"symptoms we see can be drawn about the relative welfare of in animals attemptingto get away fromaver- birds kept in cages or in pens, depending on sive situationsare also present in animals ac- which studyis cited, it is extremelyimportant

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions 314 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 to know how such apparent contradictions nase and other enzymes also showed much arise. Some answersare not hard to find.Few higherlevels in chased deer than in those that studies reportthe effectsof handling on birds were shot. These major differencesled Bate- whose blood is takenfor sampling, and do not son and Bradshaw to conclude thatdeer hunt- even state how long afterbeing caught (itself ing with hounds causes considerable suffer- a potential stressor) the blood samples were ing. As a resultof thisconclusion, the National taken.As handling affectscorticosteroid levels Trust (a major landowner in Britain) decided in the blood, it is clear that this is potentially to ban deer hunting on its land because of a major source of error.There is a naturalrise animal welfareconsiderations. and fallin hormone levels thattake place after Suppressed functioningof the immune sys- a stressfulstimulus has been applied (Wing- tem has also been suggested as an important field et al. 1997) which is oftennot taken into physiological indicator of welfare since it is account when measuring changes in cortico- so directlyrelated to susceptibilityto disease steroid levels afterexposure to environmen- which,as we have alreadyseen, is a universally tal stimuli. acknowledged measure ofpoorwelfare. More- This is not meant to implythat physiological over,suppression of immune responses seems measurements are unimportant. But it does to be affectedby glucocorticoids,natural opi- mean that, in choosing which physiological oids and other aspects of the physiological variables to use to measure poor welfare,we stressresponse (Sapolsky 1994; Toates 1995). should not relytoo heavilyon those thathap- In humans,there appears to be a demonstrated pen to have been labeled "stresshormones," linkbetween stressfullife events, immunosup- as theymay not be as specific to states of un- pression and disease, such as in the case of pleasant motivationas we mighthave thought. increased susceptibilityto colds (Andersen et Relying on conventional measures of stress al. 1994). In mice, too, social status and hor- without corroborative behavioral evidence monal stateaffect susceptibility to disease (Bar- that the animal is not merely excited at the nard et al. 1993). anticipationof pleasurable experience can be, There are verycomplex and reciprocal in- and indeed has been, verymisleading. teractionsamong the nervous,endocrine and Apart fromglucocorticoids and theirrepu- immune systems(Maier et al. 1994). The in- tationas "stresshormones," a number of other terpretationin termsof animal welfareis even physiological measurements have been used furthercomplicated because sex hormones, to assesswelfare. These include hormonessuch particularlytestosterone, also suppressthe im- as prolactin and luteinizing hormone, natu- mune system.Thus many male animals have rallyoccurring opioids such as 3-endorphins, an increased susceptibilityto diseases and par- as well as changes in neurotransmitterssuch asites during the breeding season as quite a as dopamine and noradrenaline (for reviews naturalpart of their life cycle. Indeed, one cur- see Broom and Johnson 1993 and Toates rent theoryof mate choice relies on the as- 1995). Particular interest has recently cen- sumption thatthe immune functionin breed- teredon evidence thatskeletal or heartmuscle ing males is inevitablycompromised, and that has been damaged as a resultof overexertion. females choose males that are able to over- Bateson and Bradshaw (1997) used a variety come this"handicap" (Folstadand Karter1992). of measures to argue thatred deer (Cervusela- Once again, we are cautioned about conclud- phus) in the U.K. are in a stateof physiological ing too much froma single physiologicalmea- exhaustion and show evidence of muscle dam- surement. age after being hunted with hounds, com- It is clear, then, because of the many and pared to nonhunted deer that had been shot complex ways in which physiological factors withrifles. In a typicaldeer hunt, the animals prepare the animal to respond to threats,that are chased fornearly 20 km,after which their it is verydifficult to state which ones reliably levels of plasma hemoglobin are consistent and definitivelycorrelate withstates of suffer- withconsiderable intravascularhemolysis that ing or pain thatindicate poor welfare.That is is much more severe than thatassociated with not to say,when the studies have been done, "normal" exercise in thisspecies. Creatine ki- that a physiological variable might not turn

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out to be extremelyuseful in the assessment on normally,we may in the long run take of welfare;but our confidence that it can be longer to recover,and in thissense reduce our used as such depends on extensivework that welfare.On the otherhand, therewill be other demonstratesits exclusivityto aversive situa- symptoms,such as ulcers,which are nonadap- tions, as shown by the behavior. Nor should tiveand a sign thatthe body's defense mecha- we necessarily expect any one physiological nisms have broken down. Here findingways variable to be seen in all situations that ani- to reduce pain may be the best thing to do. mals findaversive. Given thatanimals respond Since the body maynot be able to repair itself, differentlyto various threats,we may have to taking steps to make ourselves feel better by be satisfiedwith a range of differentvariables, reducing our sufferingis more likelyto lead each specificto a particularaversive situation. to a full recoverysooner. One set ofphysiological variables may be good The problem is thatalthough both cases in- measures of sufferingcaused byexhaustion as volve unpleasant feelings of illness and pain, a result of a deer being chased by dogs over in the firstinstance these indicate that adap- a period of a few hours, but quite different tive defenses are at work,whereas in the sec- measures may be appropriate for suffering ond they are a sign that the defense mecha- caused by a bird being deprived of food or a nisms have broken down. Natural defense farmanimal being kept on a bare slattedfloor mechanisms that are "unpleasant by design" for manyweeks. for adaptive reasons may outwardlyappear The second difficultywithusing physiological and inwardlyfeel the same as those of a defen- measurementsis knowingwhat level of a given sive breakdown. So where should the line be physiologicalvariable should be considered to drawn? How much in the way of natural de- indicate poor welfare. Even if one supposes fense mechanisms (e.g., a rise in heart rate or that corticosteroidhormones are the appro- corticosteroidlevels) should be seen as com- priate variable to use for assessing a situation patible withgood health and welfare?Where, thatthe animals found aversive,we would still in other words, does unacceptably poor wel- need to know how high the levels would have fare begin? to rise before we could conclude that the ani- There is, of course, no single answerto this mal's welfarewas being adverselyaffected. As The answer to the of we have seen, corticosteroidsare an important (Mendl 1991). question and adaptivepart of thebody's natural defenses whether feveris adaptive in a given instance against certain dangers,so thatwe should not is a purely empirical one: does takingaspirin conclude that anyrise was necessarilyindica- when feelingill lead to a longer or shorterpe- tive of poor welfare. But how much of a rise riod of recovery?It is not unlike the question would be indicative? ofwhether depression in humans is a defense This is essentially the same dilemma en- or a dysfunction:are people who experience countered byNesse and Williams (1995), who depression better or worse at making impor- tryto distinguishbetween responses that the tantlife decisions (Nesse and Williams 1995)? body makes to disease that are essentiallyde- It follows that questions of how much fever fense mechanisms (such as fever and pain) or how much depression should be tolerated and those that are defects (such as jaundice before attemptsare made to reduce them are and ulcers). They argue that our bodies have also empirical ones. We have to discoverwhat evolvedadaptive defense mechanisms,such as relationship a given level of malaise has to raising the body temperature when chal- otheraccepted criteriaof welfare, the mostob- lenged bydisease organisms,because thispro- vious ones being those relating to physical vides an unfavorable environmentfor those health. As we have seen repeatedly,there is no organisms. A fever is unpleasant for us but way to calibrate what level of a physiological damaging to bacteria and viruses. Feeling ill variable is compatible with good welfarejust and taking to our beds may be adaptive be- by considering it in isolation. We need either cause itforces us to restand thushasten recov- to show that the variable in question relates ery.Although we may feel better temporarily directlyto physical health or that it is linked ifwe take aspirin,reduce our fever,and carry to it indirectlyvia some other pathway.

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BEHAVIOR AND WELFARE tween two strongmotivations (e.g., to feed or Behavior has been used in the assessment to flee from the presence of a conspecific at of animal welfare in two differentways. The the food dish), and thus an animal is effec- firstis that various kinds of behavior such as tively excluded from an important activity stereotypies,redirected activities, and vacuum such as feeding. Many behavioral indicators activitieshave been used as indicatorsof poor of welfare are thereforethought to indicate welfare,somewhat in the same way as physio- frustrationor conflict.For example, Tinber- logical measurements.These behavioral indi- gen (1951) described a categoryof behavior cators are subject to the same two difficulties shown by animals when theyare in a conflict thatbeset physiologicalmeasurements, namely, which he called displacementactivities-odd or deciding which behavior to use and determin- irrelevantbehavior thatappears to have noth- ing how much of a given behavior indicates ing to do with the conflict at all. A herring "poor welfare."The second way behavior has gull in a conflictbetween attackinga rivaland been used is as a more direct readout of how fleeing, may suddenly startpulling up grass, an animal responds to a given situation,and thereby engaging in apparently irrelevant whetherthe animal findsit aversive or pleasur- nest-buildingbehavior in the middle ofa fight. able. We have seen in the previoussection that Since there is considerable evidence that dis- many of the physiological symptomsthat ac- placement activitiesoccur in situationsof con- company pain and sufferingare similar to flict and tension, Maestripieri et al. (1992) those thataccompany pleasure. Since the dis- suggested that such "irrelevant" behaviors tinction between pain and pleasure is obvi- mighthave considerable value as indicatorsof ously criticalto the assessmentof welfare,the emotional conflict.Another indication that behavioral distinctionbetween aversion (that an animal is highly aroused is when captive is, an animal will work to get awayfrom it) or animals go through complete behavioral se- pleasure (an animal will work to gain or con- quences even when the usual stimulieliciting tinue withit) is one of the most criticalones such behavior are not present. Hens kept on that can be made. The animal's own choices wire-flooredcages will go through all the and preferences are thus seen not merely as movementsof dustbathing(Vestergaard 1980) peripheral and perhaps sentimentalluxuries even though thereis no loose substrateon the that are less importantthan "objective" mea- floorand no dust reaches the feathers.Lorenz sures such as stresshormones, but ratheras an (1950) called such behavior vacuum activities indispensable part of welfareassessment, and because they are performed "in a vacuum," criticalto the correctinterpretation of almost thatis, in the absence ofany external releasing everyother criterion.Below I will outline how stimuli.To Lorenz and others who accepted behavior has been used in this firstway, but his energymodel of the controlof motivation, then concentrate on its second and, in my the presence of vacuum activitiesindicated a view,much more criticalrole as the keyindica- high level of frustration,and thereforepoor tor of pleasure or suffering. welfare (e.g., Sambraus 1982). Even if it is not strictlycorrect to say that BehavioralIndicators such behavior is elicited in the absence of all It is assumed thatpoor welfareoften results external stimuli (caged hens oftenflick food when animals are preventedfrom expressing onto theirheads and thusmay gain some stim- highlymotivated behavior (Dawkins 1988), ei- ulation relevant to dustbathing), it is never- therbecause the relevantexternal stimuliare theless true thatcaptive animals mayperform absent or because the confinesof a cage physi- behaviors to apparentlyreduced levels of ex- callyprevent them fromdoing so. One justifi- ternalstimulation. Although thismay indicate cation forusing a particularbehavior as a mea- a degree of frustration,it does not followthat sure of welfare is that it indicates when an the animal's welfareis necessarilypoor, since animal is highlymotivated, but frustratedor the performance of a vacuum activitymay it- thwartedin itsattempts to accomplish a behav- self be an adequate substitutefor the real ior. Alternatively,even when it might not be thing.Pet dogs chase balls, but we do not con- limited physically,there may be a conflictbe- clude thereforethat theirwelfare is reduced

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions SEPTEMBER 1998 EVOLUTION AND ANIMAL WELFARE 317 because theymay be deprived of hunting be- courtship displays. Indeed, stereotypyhas in havior. On the contrary,chasing balls seems the past been viewed as an evolutionarypres- to be highlyreinforcing and generallyan ade- sure on signals to make them less ambiguous quate substitutefor hunting prey. Once again, (Cullen 1966). In the context of animal wel- as withmany of the physiologicalmeasures dis- fare,however, the definingfeature of a stereo- cussed earlier,the occurrence of substituteor typyis notjust itsfixed nature but itsapparent vacuum activitiesin itself does not indicate lack of function.Swaying to and froor pacing poor welfare.It should alert us to the possibil- round and round a small cage does not itythat an animal is highlymotivated to behave achieve anythingfor the animal, and yetit con- in a certainway but, without further investiga- tinues to do it. tion of how that behavior is controlled and The causal basis of stereotypies,as well as what turnsit on and off,that behavior cannot exactlywhat they indicate about the welfareof lead us to conclude thatthe welfareof the ani- animals,is a matterof continuingdebate. One mal has necessarilybeen compromised. complication is that the earlydevelopment of Even greater caution should be applied to a stereotypymay be owing to factorsdifferent labelinga behavior"abnormal" because it looks fromthose thatmaintain it in an adult animal odd, and then assuming thatall abnormal be- (Lawrence and Terlouw 1993; Mason and Tur- havior is indicativeof poor welfare.Some ab- ner 1993). Hens in small cages may develop normal behavior,such as self-mutilations(e.g., stereotypicpacing back and forth,apparently featherplucking in parrots),are clearlyan in- out of frustratedattempts to escape (Duncan dication thatall is notwell,but not because the and Wood-Gush 1972). Even when let out of behavioris abnormal in the sense of "different their cages, however, they may continue to from average" or even "not seen in wild ani- show the same stereotypedbehavior. So a ster- mals" (Mason 1991). Rather,it is indicativeof eotypymay not necessarilyindicate any cur- poor welfarebecause it resultsin injury,thus rent adverse conditions. Rather, it may indi- anchoring it firmlyto the veryfirst criterion cate that at some time in the past, its welfare we considered. Other abnormal behavior (in was compromised and that the animal is still the sense of "away from the norm") may be affectedby thatpast experience. completelycompatible withgood welfare.For Anotherproblem withthe interpretationof example, the behavior ofpets towardshumans stereotypiesis thatthey may even help the ani- (and vice versa) can be extremelyabnormal mal cope with its environment,in the same withoutany suggestion that the welfareof ei- way perhaps, that pacing up and down for a therparty has been compromised. human sometimes relieves tension. There is There is, however, one categoryof abnor- some suggestion that stereotypiesare associ- mal behavior thathas attracteda great deal of ated witha reductionof some of the physiolog- attention as an important indicator of poor ical symptomsof stress,such as corticosteroid welfare.Stereotypies are fixed sequences of be- levels or heart rate. Cronin et al. (1985) even havior performedover and over again in the proposed that by performing stereotypies same way with no obvious function (Mason such as bar-biting,pigs induce a state of self- 1991; Lawrence and Rushen 1993). For exam- narcotization through the release of endor- ple, polar bears and foxes in zoo enclosures phins into the bloodstream. We should not maystand swayingtheir heads and necks from conclude, however,that stereotypies maintain side to side or may pace around a set route so the physiological balance of the animal and often that theywear away the ground. Sows thusare no cause forconcern. Rather,viewing confined in stalls may constantlyrub their them in an evolutionarycontext suggeststhat mouths back and forthover the bars, doing theymay be failed attemptson the part of an thisso oftenthat they make themselvesbleed. animal to alter its environmentin some way. The term "stereotypy"is in many waysan un- For example, behavior such as gnawing,push- fortunateone because it would seem to imply ing or running may be adaptive in the sense the fixedor stereotypicnature of the sequence that theyincrease an animal's chances of es- being performed,which would include many cape in manynatural situations. In a small cage quite naturalsequences such as breathingand where escape is impossible,however, they may

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be totallyineffective, and yet repeated over such as an infant calling to its parents, or and over again by the animal, so that theyap- among very highly social animals that aid pear to be functionless stereotypies,albeit other members of theirgroup. witha functionalorigin. Repetition of behav- During tonic immobility,sometimes called ior that does not fulfillits evolutionaryrole animal hypnosis(Eddy and Gallup 1994), ani- is widelybelieved to indicate poor welfareat mals remain absolutely motionless, notably some stage in the animal's life (Dantzer 1991; when handled. In chickens,it consistsof lying Broom andJohnson 1993; Mason 1993). on theirbacks in a rigid and frozen position, Still another indication of poor welfareis a but versions of "frozen"and apparentlyhyp- change in activitylevels, that is, changes in an notized postures are seen in a wide varietyof animal's movement-either how it carriesout animals. It appears to be an antipredatorre- a behavior or how long it takes to do it. Cattle sponse when an animal is captured, and the kept on slatted or slipperyfloors may take up only defense is to "play dead." The duration to 20 minutes to lie down, whereas theytake of tonic immobility-the time fromits induc- onlya fewseconds on a nonslipperyfloor (An- tion to the animal rightingitself-has been dreae and Smidt 1982), stronglysuggesting used as a measure of fearfulness(Jones and considerable discomforton the slatted floor. Faure 1981; Vestergaardet al. 1993). The unusual gait and general difficultieswith Many different behavioral indices have standingor walkinghas been noted as an out- been proposed and certainlyhave their uses ward sign of bone abnormalitiesin intensively in the assessmentof welfare,but theyare sub- keptbroiler chickens (Wong-Valleet al. 1993) ject to the same twoproblems thatwere raised and turkeys(Nestor 1984). More positively, in connection with physiological indices- since play behavior is associated withphysical namely, that although they may under some health (Fagen 1981; Martin and Caro 1985; circumstancesindicate that an animal's wel- Bekoffand Byers1992) it has been suggested fare has diminished, their interpretationis that the presence of this behavior should be subject to doubt; even where some impair- taken as a sign of good welfarein captive ani- ment of welfare is indicated, it is difficultto mals,particularly young ones (Lawrence 1987). know how much. Broom andJohnson (1993) The idea thatan animal's vocalizationsmight proposed that if an animal shows stereotypic provide an indication of its state of welfareis behavior more than 40% of the time, then it an attractiveone. Calls are easy to record and is suffering,but this figureis somewhat arbi- quantify,and as communication signals they trary.We stillneed a wayof anchoring the be- mayhave evolved speciallyto indicate "need," havioralsymptoms of aversivenessof a situation particularlyfrom young animals to their par- to the animal, and a frameworkfor deciding ents (Godfray1991). Wearyand Fraser (1995) how the differentconstituent indicators can showed thatwhat theycalled nonthrivingpig- be linked together.I shall argue thatthe unify- lets (lightweightandlowweightgain) andpig- ing frameworkis the animal's systemof prefer- lets thathad not been fed forsome time gave ence and choice. higher frequencycalls than those from thriv- ing and well-fedpiglets. Domestic chicks give Choice,Reinforcement and Welfare high-pitchedand piercing"distress" calls when In humans, reduced welfareresults from a isolated or cold (Wood-Gush 1971) and the variety of circumstances. Exhaustion from ultrasoniccalls of ratpups increase when they overwork,boredom from not enough to do, become chilled (Olivier et al. 1994). Weary fear from hearing an intruderin the house, and Fraser thereforesuggest that such calls or prolonged thirstare all unpleasant and, if can be used as measures of the welfare of a protracted,likely to lead to reduced welfare, particularanimal. but theyare all different.They resultin various While such vocalizations may be extremely physiological responses and have diverse be- valuable as indicators of need in young ani- havioral responses as well. About the only mals, they can be expected to be confined thing theyhave in common is theyall spur us mostlyto situationswhere the one calling en- to removeourselves from those situations,and deavors to summon the aid of another animal, to striveto avoid the same situationsin future.

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In otherwords, they are all aversive,as demon- when an animal is hidden frompredators alto- strated by our reactions. The importance of gether. These are all adaptiveexplanations. If knowingwhether an animal, human or non- we look at the mechanismsby which such adap- human, shows byits behaviorwhether it findsa tivechoices are made, however,we can posit a situationaversive becomes apparent when we wide varietyof possibilitiesranging from simple observetwo people ridinga rollercoaster. Both fixed rules to a complex moment-to-moment are screaming, both have pounding hearts evaluation of differentoutcomes. and a rush of adrenaline, but perhaps one has The simplestmechanisms are tropismsand been dragged unwillinglyonto the ride and is taxes in which orientation toward or away genuinelyfrightened, whereas the otherenthu- from a stimulusis achieved by linkingrecep- siasticallyclimbed aboard and is enjoyingthe tors to a response mechanism. Such mecha- ride greatly.Operationally, we can distinguish nisms are found in both animals and plants, them bywhether they freely choose to have a but theytend to giverise to veryfixed responses, second ride. For the firstperson, the ride is such as movement toward light or nutrients. clearlyaversive and mayhave givenrise to gen- With many animals, however, natural selec- uine suffering.For the second, it provided tion has enabled them to respond much more positivereinforcement. It has been suggested flexiblythrough a systemof positive (reward- thatsimilar logic maybe used withnonhuman ing) and negative(punishing) reinforcers.Ani- animals to distinguishbetween situationsthat mals can learnresponses that provide rewarding theyfind pleasurable or reinforcingand those experiences associated withincreased fitness, that theyfind aversive (Dawkins 1990). but theycan also learn negative responses to There are two issues here. One is how an stimuli associated with reduced fitness.The animal's choice and reinforcementmecha- importantpoint is that an animal using a sys- nisms are related to health and welfare.The tem of reinforcersand learned associations second is whetherthe subjectivehuman expe- will, like the simpler animal or plant with its riences of "suffering"that often accompany tropismsand taxes,be able to avoid predators negativereinforcement or absence of positive and findfood, but will be much more flexible reinforcement(such as in pain or lack of food) because it can tryto take a much wider range are also presentin nonhuman animals in aver- of other responses in case offailure. It willalso sive situations.In keeping with my intention be able to decide betweenvery different courses to separate such questions, I shall here con- of action by weighing the reward (or punish- centrate on the firstand postpone discussion ment) value of differentones (Rolls 1990). of the second until later, startingwith a view For example, the tasteof waterwould provide of how animal choice and reinforcement a greaterreward for a verythirsty animal than mechanisms have evolved as part of adaptive a moderatelysweet taste to a well-fedone. To behavioral strategies. make sure thatrewards are appropriatelycho- Natural selection has led to the evolutionof sen, they need to be evaluated on a similar some behavioral mechanismsthat help ensure scale that will accuratelyassess the costs and the survivalof the body,while othersfavor re- benefits of obtaining them at that moment productivesuccess, even at the riskof the indi- (Houston and MacNamara 1988). Reward vidual's survival.Some of these mechanisms and punishment signals provide a common are concerned withavoiding damage or injury currencyfor helping an animal decide which to the bodywhen the danger is alreadypresent action to take at a given time (Rolls 1998). (forexample, protectinga limb fromlikely in- This has importantimplications for animal jury). Others are concerned withavoidance of welfare because reinforcersmay become im- a situation entirelywhen damage or injuryis portant to the animal, quite apart fromtheir likely.An example of such avoidance would fitnessconsequences. Thus, if seeking cover be movingaway when a predator appeared on in nature is an importantantipredator adapta- a distanthillside, long before a chase was initi- tion fora small mammal, and hence positively ated. Still other avoidance tactics are used reinforcing,then such an animal in a preda- even earlier in time, such as a preferencefor tor-freecaptive environment may find that sleeping during the day in dense vegetation, seeking cover is positivelyreinforcing whereas

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions 320 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 absence of cover is veryaversive, even though what it finds aversive (Dawkins 1990). If the its fitnessin captivityis not increased by seek- animal shows littleevidence of being able to ing cover.Its welfare could, however,be signif- change its circumstances,then probably the icantlyreduced ifno cover were provided. In- change willmake littledifference to itswelfare. deed, I will go one stage furtherand argue But if the animal will literally"do anything"to that,apart fromovert health problems, most get somethingit wants,or to escape fromthe of the concerns about animal welfarearise be- conditionsin whichit is being held, the change cause of reinforcementmechanisms-that is, may be very important.An animal that will animals find some situations highly aversive push heavyweights, give large numbers of ar- and are unable to fulfillthe conditionsthat are bitraryresponses (such as pecking a key or specifiedby their reinforcement mechanisms. pressinga lever), cross an electricgrid or oth- The evolution of positiveand negativerein- erwisegive high priorityto obtaininga positive forcers that allow flexibilityof behavior and reinforcer or getting away from a negative the acquisition of new responses thus has a one, is demonstratingthe value it places on cost: animals may find certain circumstances thatreinforcer. Matthews and Ladewig (1994) very negativelyreinforcing even when their used the number of presses on a nose plate health or fitnessis not actually threatened. that pigs made as the response with either The caged animal kept withoutcover has re- food or social contact withanother pig as the duced welfare by being continuouslyfearful reward. When they increased the "price" by even though its welfare (as judged by health making the pigs push the plate notjust once and fitnessprospects) are good. The means but up to 30 timesfor each reward,they founid of increasingfitness in the wild (through fear that the pigs were willing to pay the higher that results in escape for instance) becomes price forfood and worked harder and harder part of whatwe thenjudge to be reduced wel- for the same number of rewards.By contrast, fare. It followsthat good welfareinvolves not when social contactwas the reward,ihey found only good health and prospects for future that the pigs did not work as hard and thus health as judged by a human observer, but obtained fewerrewards. Despite the difficul- good welfareas perceivedby the animal. If a cage ties that clearlyexist with this approach (e.g., without cover is perceived by the animal as Dawkins 1990, 1997; Houston 1997; Mason et highlyaversive; then there is less than good al. 1998), thismethod is stillthe only one that welfare,even fora healthyanimal. endeavorsto show the animal's "pointof view." As argued earlier,we have rio a prioriway of Choice and reinforcementmechanisms thus knowingwhat will be positivelyor negatively occupy a veryspecial place in the evaluation reinforcingto an animal, or even whetheran of animal welfare. animal is able to associate a specificresponse At the same time, however,it is important withobtaining or avoiding a given reinforcer. not to put too much emphasis on whatanimals Such insightshave to be establishedby experi- mayor maynot findreinforcing. By now itwill ment. As we have also seen, the physiological be quite clear that animals do not alwaysact measurementsthat have been made so farare to benefittheir fitness. This will be true even almostall of the activationor exhaustionof the under natural conditions. For example, a mi- motor side of the system,not of the decision- gratingwildebeest may choose to cross a river, makingreinforcement mechanisms themselves. but then is eaten by a crocodile. On average, Until we have brain-scanor other techniques migration-including crossingrivers-is ben- for deciding whether an animal evaluates a eficial,but sometimes it isn't, even in natural given situation as aversiveor pleasurable, we environments(RDawkins 1982). In unnatural must relyon the behavior of the animal itself environments,however, the likelihood of an and, in particular,on its choice behavior and animal choosing an option thatlowers rather its abilityto associate arbitraryresponses with than raisesits long-term fitness becomes much rewardsand punishments. greater, because it is more likely to be con- Furthermore, we also have to establish frontedwith a range of options forwhich it is whether a given reinforcerwill cause an ani- not adapted. Its ancestors may have lived in mal to obtain whatit needs or to get awayfrom environmentsin whichabsence of covermeant

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death by predation, and only those survived abilityto carryout itswork is reduced ifa part thatremained hidden. Unnaturalenvironments is broken or damaged. An injured animal's fit- may also lead animals to make inappropriate ness is directlyreduced, for instance, if it can choices. For example, an animal may find a no longer flee frompredators. For thisreason, sweet taste highlyreinforcing because (in an I have stressed the importance of veterinary adaptive sense) in itsnatural environment this evidence about good or poor health as the first preferenceled it to seek out fruitand honey. and essentialmeasure of welfare.Animals have In a captive environment,however, the rein- evolved a number of mechanisms,however, to forcingproperties of a sweet taste could lead avoid gettingthemselves into such dire straits it either to ingest nonnutritivesaccharine or in the firstplace. These include mobilizingthe to overconsume freelyavailable sucrose, nei- HPA systemand changing their glucose me- ther of which would increase its fitness. tabolism so that they are better able to run What animals findpositively and negatively away from danger; such mechanisms enable reinforcingshould thereforenot be used in animals to avoid dangerous situations, and isolation as a measure of welfare,any more even play "Russian Roulette" with their im- than any other single measure should be. But mune systems,in the interestsof reproduc- knowing what animals find pleasurable or tion. Such mechanisms-ones thatcome into aversiveoften allows us to make sense of other play before (or to avoid) primarythreats to measures such as physiologicalchanges. What fitness-can lead to secondaryconsequiences. the animal prefersand will work for (or get Secondarymeasures of welfare orperceived threats away from) is thus not a luxuryto be tagged tofitness may be activated when the animal's on to other more "real" measurements such health is stillgood, and skepticsmay then ar- as physiologicalparameters, but is completely gue thatthere is no welfareproblem, thuscon- centralto the proper evaluation of all welfare. fusingthe issue. Since the animal is behaving It is whatdistinguishes animals and plants and as ifits fitnesswere threatened,however, and givesrise to our moral concern foranimal wel- eithertaking or attemptingavoidance actions, fare. It helps us to make sense of other mea- its welfaremay be reduced just as much as if sures,and providesa frameworkin which they fora primarythreat already evident.As Hofer can be evaluated. and East (1998) put it: "Naturalselection max- imisesfitness but not necessarilythe well-being CONCLUSIONS ABOUT of organisms."A major problem, but no worse METHODS OF ASSESSMENT than thatencountered by Nesse and Williams I have argued thatapplied welfareresearch (1995) in theirdiscussion of human medicine, stands to benefit greatlyby becoming more is distinguishingbetween cases where the sec- Darwinian in its outlook. Essentially, this ondary mechanisms are effective(i.e., where means pursuing the consequences of viewing the behavior or physiologicalmechanisms are the so-called indicators of welfare as adapta- the animal's way of dealing or coping witha tions to deal with threatsto the animal's fit- danger) and where secondarymechanisms are ness, subject alwaysto the provisothat adapta- ineffectiveand pathological.Clearly, interven- tionscan onlybe understoodin the contextof tion to "preventsuffering" is much more ap- the environmentin which theywere evolved. propriate in the second case than in the first. To be more explicit,I will argue thatthe most There are a number of important conse- practically useful and evolutionarilyimpor- quences of taking this Darwinian view of ani- tant measures of welfarefall into two catego- mal welfare: ries: primarymeasures that are direct threats 1. High priorityshould alwaysbe given to to fitness,and secondary ones that are per- primarythreats to fitness(i.e., veterinary ceived as threatsto fitness. measures of welfare) since these have Primarymeasures of welfare include such fac- been major selectiveforces in the livesof tors as injury,disease, exhaustion of muscle all animals. tissue,and dehydration.Here an animal's abil- 2. Individual secondary measures of wel- ity to survive and reproduce is directlyre- fareshould not bejudged to be "unrelia- duced, in much the same waythat a machine's ble" just because they do not correlate

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consistentlywith primary measures. Ani- foraction to gain somethingthe animal mals usually have more than one kind wants,and preparation for action to es- of danger to avoid. They have complex cape something it finds aversive. The tradeoffsat all levels in order to mini- same limbsand muscles are used in both mize reductions of fitness in facing a behaviors, together with the same en- wide range of threats.At differenttimes ergyneeds. The differenceis whetheran of the day or year, or depending on ex- animal decides that a given situation is ternalcircumstances, they will reallocate positivelyor negativelyreinforcing. Thus, priorities:For example, animals mayde- particular emphasis should be given to pressor enhance theirimmune responses, an animal's own choice and reinforce- increase or decrease their physiological ment mechanisms; although these are "stress"responses, or find some stimuli not an infallibleguide to welfarein them- moreor lessaversive. Such changesshould selves,they do allow us to make sense of not be seen as a nuisance or inconsistent all the other measures. They tell us what with primarymeasures (although they the animal finds rewardingor aversive. may well complicate the interpretation And by findingout how hard an animal of an animal's welfare). Rather, theyre- will work to change its situation,we can sult fromthe complexityof an animal's learn somethingabout the strengthof its adaptive response to various dangers. motivationto change. The finelytuned 3. We should not expect that the response systemof primaryand secondary rein- to all dangers should be the same. Given forcementsthat have evolvedthat enable that the most adaptive response (at all animals to deal withthe costs and bene- levels in the body) mayvary, depending fitsof differentcourses of action are a on whetherthe danger is fromdehydra- major secondary mechanism for avoid- tion,disease or predatorattack, it is most ing primarythreats to fitness.As such, unlikelythat there will be a single mea- theyconstitute both our best chance to sure ofpoor welfare,even a multicompo- viewthe way another species perceivesits nent one, that can be identified in all world and, ironically,a major source of cases where the fitnessof the animal is poor welfare in themselves. If animals actually or potentially compromised. did not perceive various situations as Rather, the responses of a given species "punishing,"assessing their welfare would should be studied separately when it be quite easy. meets threatsof predation,dehydration, Although insightsfrom evolutionarybiol- or absence of social companions. It may ogy can thus benefit applied animal welfare turn out, when the behavioral, physio- studies,other areas of biologycan also benefit logical and biochemical data fromthese fromsome of the issues raised by animal wel- various situationsare analysed and com- fare.Indeed, it could be argued thatattempts pared, thatthey will have a common com- to find valid ways of measuring welfare have ponent or syndromeof poor welfarethat thrown into sharp relief some important is- can be identified.This should be regarded sues: how is behavior controlled,how do hor- as a fortunateand even somewhat sur- mones such as corticosteroidsfunction in the prisingfinding, however, and not some- body, and how are animal decision-making thingto be expected in advance. mechanismsrelated to fitnessin the long tenn? 4. Particular effortsshould be made to Above all, issues of animal welfareforce us identifythe common components of sit- to look at consciousness and its evolution. In uations that animals find aversivefrom almost all other areas of biology, questions those thatthey find pleasurable. No indi- about consciousness can be put to one side cator of stressor poor welfareshould be in the best behavioristmanner. Learning and labeled as such unless it is clearlymore reinforcementmechanisms (and even emo- than a symptomof excitementor readi- tions) can be discussed independently of ness for action. In animals there is con- whetheranimals are consciouslyaware ofwhat siderable overlap between preparation theyare doing. But a concern foranimal wel-

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions SEPTEMBER 1998 EVOLUTION AND ANIMAL WELFARE 323 fare does not permit such a convenient eva- humans respond to certain situationssuch as sion. Our own consciousness is an ever-pres- hunger and cold (Cabanac 1992), it does not ent reality.If we believe in the explanatory follow thatboth species are consciouslyexpe- power of natural selection,we have at the very riencing hunger and cold. Even the fact that least to consider the possibilitythat conscious- humans saythey are consciouslyexperiencing ness evolved bynatural selection. If so, it must "suffering"from cold and then proceed to be- either be a factorin the life of an organism, have like rats in seeking warmth,does not or be a most extraordinaryepiphenomenon mean thatrats also consciouslyexperience the (Dawkins 1993). But ifconsciousness has phe- same thing,tempting as it is to conclude that notypic effects,it should be possible to find theydo (Dawkins 1993). The reason whysuch out what these are, and to discoverwhat is dif- a conclusion would be invalid is both instruc- ferentabout organismsthat possess it. This in tiveand subtle. turnleads to questions about how to find out One of the findingsthat has emerged from which organismshave conscious experiences. recent neurophysiologicalresearch is the con- Practical problems of animal welfare thus cept of "multiple routes to action"-the idea forcea radical reevaluationof what constitute thatthe same action can be ordered by differ- legitimatetopics of biological research,as well ent partsof the brain,some of themgiving rise as linkdiverse fields from molecular immunol- to conscious experiences and othersresulting ogy to behavior,all of which contributeto the in quite automatic responses when people re- common goal of understanding the range port no conscious experiences (Rolls 1998). of fitness-enhancingmechanisms that have An obvious example is driving a car; some- evolved in animals. As a frameworkfor a timeswe can be conscious of everyaction, and broadly based mechanistic biology, animal at other timeswe are effectivelyon "autopilot" welfareis central to much of modern biology, and not conscious of what we are doing. The even though "pure" biologistsmay not always importantpoint is that when our actions are realize it. All branches of biology are affected under conscious control, we do not lose the by the issues raised in animal welfare. unconscious pathways.On the contrary,we re- tain them,often reverting to them forroutine THE CONNECTION BETWEEN actions thatwe have done many timesbefore; WELFARE AND "SUFFERING" we use the conscious pathwaysonly for dealing In a thoughtfuland provocativeessay, enti- with novel situations. Indeed, our conscious tled "The mythof animal suffering,"Bermond minds are often not as good at dealing with (1997) correctlypoints out that none of the routine tasksas takingthe unconscious route methods proposed so farfor assessing"suffer- (Baars 1988). So the fact thatwe share many ing" in animals actuallydo so. "Suffering,"as physiologicalmechanisms and behavioral re- applied to humans, means conscious experi- sponses withother species, particularlymam- ence of something very unpleasant. Strictly mals, cannot be used as conclusive evidence speaking, none of the measures of "poor wel- that they share our conscious experiences, fare"or "stress"discussed so fardemonstrates too. It would be possible to argue that they the presence of comparable states in nonhu- simplyuse the same neural pathwaysthat we man animals. They could all be occurring in use for automatic,unconscious actions. They organismswithout consciousness thatare pro- maypossess manysimilarities to ourselves,but grammed in various ways to respond adap- not that of shared conscious experiences. tivelyas far as the animal's fitness is con- With a brain and an abilityto thinkahead ten cerned. As we have seen, adaptive responses years,you maydecide to take out health insur- to a range of stressorsoccur in plants as well ance or make other provisionsfor the future. as animals. Even measures thatdistinguish re- But thisdoes not mean thatyour pain mecha- sponses to danger in animals from those of nismsor injuryresponses become redundant, plants-namely, the abilityto show reinforced or that you should stop avoiding situations behavior-carry no necessaryimplications of thatare likelyto lead to injury.The death-defy- conscious experience. Although there are ing, fitness-increasingmechanisms we share strikingsimilarities between the way rats and with other animals could simply have been

This content downloaded from 129.67.117.205 on Fri, 19 Jul 2013 06:03:00 AM All use subject to JSTOR Terms and Conditions 324 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 73 augmentedby a consciousability to plan ration- ityto deal with longer time scales or greater ally for the future.The abilityto avoid injury complexity. thatwe see in manyspecies, throughtheir fear All this emphasizes that consciousness re- or theirability to be aware ofimpending doom mains "the hard problem" of biology (Shear has enabled us to lessen the chances of fitness 1997). Easy (although often complex) prob- reductionor avoid danger entirelysome weeks, lems are questions such as how animals dis- months,or years before danger appears. The criminatedifferent objects or how behavior is question is thusnotwhether there are similari- controlled.The hard problem is why,when we ties between humans and other species in re- make a discrimination,it feels like anythingat sponses to dangerous or aversive situations all. Why,in other words,does pain hurt? (because there clearlyare), but whichsimilari- The fact that we cannot yet solve the hard ties are specificallyrelevant to the likelihood problem does not mean that we should rule of shared conscious experiences. out the possibilityof including it some day in Bermond himselfargues that both a well- the science of animal welfare.The currentstate developed prefrontalcortex and a rightneo- of animal welfareis the studyof health,fitness cortex structureare necessaryand therefore and the various mechanisms animals have thatconscious emotional experiences are only evolvedfor ensuring future health and fitness. to be expected in anthropoid apes and possi- Such studies can be carried out without any blydolphins. Such a hardware-dependentex- mentionof the conscious experienceof "suffer- planation assumes, of course, that conscious ing." But a complete science of animal welfare experiencesare unique toparticular brain struc- would include a considerationof the conscious tures,and ignoresthe possibilitythat in species experiences of animals, just as a complete verydifferent from us, other brain pathways studyof biologywould. To thatextent, biology could give rise to consciousness by using dif- is incomplete, too. Animal welfarestudies, by ferenthardware. Even the determinedlyDar- focusingon thefeelings an animalmight experi- winian view that if consciousness evolved by ence, have brought a whole new dimension natural selection it must have a detectable ef- to the study of animal consciousness, which fect on some aspect of an animal's behavior otherwiseemphasizes purely the intellectual or physiology,and do something to enhance achievements of animals as the key to under- fitness(Dawkins 1993), does not free us from standing their consciousness (Griffin1992; this dilemma. If consciousness enhances ex- Bekoffand Jamieson 1996). Cognitive ethol- isting danger-avoiding and reward-seeking ogy emphasizes cognitiveabilities, whereas in mechanisms byenabling them to operate ear- the context of animal welfare,emotions are lier and earlier,it is verydifficult to see where more important.The often quoted phrase of unconscious learning mechanisms are re- JeremyBentham is relevanthere: "The ques- placed by conscious experiences. It mightbe tion is not Can they Reason?, nor Can they thatconscious experiences or qualia are pres- Talk? but Can theySuffer?" The question Ben- ent in many animals which "feel" hunger or thamhad in mind was thatof which organisms fear in verymuch the waywe do. But it could deserve moral consideration, but it could also be, forthose who wish to take a hard line, equally well be used as to mean the question that the basic physiological and behavioral ofwhich animals mightpossess consciousness. mechanismswere in place and fullyfunctional The key to the origin of consciousness itself long before consciousness evolved, and all maylie in the emotional experience of suffer- thatconsciousness did was to add an extraabil- ing (Dawkins 1993).

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