Between Physiology and Psychology—Ethology and Animal Feelings

Abstract

This chapter explores scientific thinking about animal behaviour and welfare from the late nineteenth century onwards. After a period of unsystematic investigations of animal cognition and feelings (affective states), many researchers abandoned allegedly anthropomorphic approaches in favour of new mechanistic behaviourist models. Interest in the evolutionary roots and purpose of behaviour was gradually revived by ethologists from the interwar period onwards. While senior continental ethologists shied away from research on animal feelings, a growing number of Anglo-American ethologists questioned supposed divides between animal and human cognition and anthropomorphic taboos associated with studying affective states. In post-war Britain, the University Federation of Animal Welfare and ethologists Julian Huxley and William Homan Thorpe used research on behaviour and stress to call for improved welfare. Their actions were strongly influenced by Edwardian concepts of science as a progressive force for the moral and spiritual improvement of human society.

There is a long history of thinking about animals, their emotional states, and humans’ duties towards the creatures in their care. For centuries, European thought was primarily influenced by the twin Christian concepts of humans’ mastery over animals and animals’ status as fellow creations of God. However, from the Early Modern period onwards, secularisation’s gradual disenchantment of the world began to necessitate new concepts of animals’ ontological, ethical, and legal status.¹ The modern recalibration of animals’ societal status coincided with growing interest in animals’ biological origins and behavioural characteristics. From the mid-twentieth century onwards, ethology emerged as an important new discipline explaining the roots and functioning of animal behaviour—and the welfare obligations resulting from it.

In nineteenth-century Britain, naturalists had already become intrigued by similarities between animal and human expression. Political affiliations exerted a strong influence on resulting theories about the natural world. In 1855, liberal utilitarian Herbert Spencer proposed that ‘feelings’ alongside memory and reason enabled animals to adapt flexibly rather than just reflexively to their environment. All three characteristics played an important role in his Lamarckian theory of ‘progressive’ adaptive evolution.² Published one year after The Descent of Man in 1872, Darwin’s The Expression of Emotions in Man and Animals provided detailed accounts of communicative behaviour in animals and humans. For the abolitionist Darwin, studying animal behaviour not only cast light on puzzling aspects of sexual selection but also served to highlight evolutionary continuities between species and the universality of humans.³ Darwin’s pupil, George Romanes, went on to explore links between animal and human consciousness and devised an evolutionary tree based on intelligence. Romanes’ attempts to prove Darwinian evolution via comparative psychology led to the publication of Animal Intelligence in 1878⁴ and Mental Evolution of Animals in 1883.⁵

The often-anecdotal way in which Darwin and Romanes mobilised evidence on animal behaviour proved controversial.⁶ Although he also argued that animal cognition could be a positive evolutionary force, British psychologist and zoologist Conwy Lloyd Morgan became concerned about vague methodologies. Around 1900, he coined what became known as Morgan’s Canon while studying relations between animal habit and instinct. Trying to put animal psychology and behavioural research on a more expert-based ‘scientific’ footing, Morgan stated that no animal activity should automatically be interpreted as a higher psychological process if it could also be explained by ‘lower’ processes of psychological evolution and development.⁷ In other words, one should not by default attribute “higher” human concepts of rationality, purposiveness, or affection to animal behaviour if this behaviour could also result from simple trial-and-error learning.⁸

While Morgan remained interested in animal psychology and cognition, other researchers attempted to show that many alleged instances of animal consciousness or voluntary behaviour were in fact due to physiological functions.⁹ Mirroring a more general shift of biological research towards quantitative laboratory-based methods,¹⁰ their work formed part of a growing backlash against ‘unscientific’ anthropomorphism. Around 1900, two researchers in particular laid the groundwork for a new era of mechanistic rather than introspective explanations of animal behaviour. In Russia, physiologist Ivan Petrovich Pavlov conducted iconic experiments on dogs, who salivated when hearing a bell associated with food (classical conditioning). In the US, psychologist Edward Lee Thorndike used puzzle boxes and mazes to measure cumulative animal learning (operant conditioning).¹¹ Animals’ behaviour could be explained as resulting either from reflexes to certain environmental stimuli and motivational states or from controlling stimuli anchored in an individual’s history. Focusing on animal cognition or affective states was unnecessary. Coined by US psychologist John Broadus Watson in 1913, a new school of ‘behaviourists’ tried to use predominantly mechanistic models to establish the behavioural disciplines as fully fledged natural sciences. In its most radical form, behaviourism—as promulgated by Burrhus Frederic Skinner in the US—completely discounted concepts of animal cognition and affective states that could not be tested experimentally.¹²

Although it dominated American research on mental states until the 1950s, behaviourism’s authority was never absolute. On both sides of the Atlantic, competing fields like animal psychology or hybridised forms of behaviourism continued to evolve.¹³ In 1917, German Gestalt psychologist Wolfgang Köhler highlighted instances of insight learning by chimpanzees on Tenerife, whose ability to use poles and stack boxes to reach bananas seemed not to stem from cumulative trial-and-error learning but from the internal realisation of a solution.¹⁴ In the US, psychologist William McDougall posited that animal instincts were more than mere reflexes and could be informed, motivated, and modulated by subjective experiences (emotions).¹⁵ At Cornell, psychobiologist Howard Liddell pioneered the comparative study of neuroses in animals and humans.¹⁶

Another group of researchers used approaches from field studies and comparative psychology to study innate and acquired animal behaviours in relatively ‘natural’ conditions.¹⁷ Applying evolutionary theory to account for behavioural continuities among related species, so-called ethologists were interested both in the biological usefulness of instinctive behaviour and in some animals’ ability to adaptively modify behaviour and acquire new knowledge via learning. Building on earlier work by naturalists and psychologists like Oskar Heinroth and Edmund Selous, their findings led ethologists to challenge purely mechanistic concepts of behaviour.¹⁸

Between the 1910s and 1930s, zoologist Julian Huxley conducted pioneering research on the ritualised behaviour of birds, including great crested grebes. Huxley linked observed behavioural patterns to Darwinian evolutionary theory but challenged parts of Darwin’s theory of sexual selection by noting that ritualised behaviour linked to courtship continued after pair formation and reproduction. He also noted that long-term sexual selection for certain traits might not always be beneficial for non-reproductive fitness.¹⁹

However, it was in continental Europe that ethology would truly take off. In 1920s’ Austria, biologist Karl von Frisch described colour perception, orientation, dance-like communication, and dialects among honeybees.²⁰ A few years later, his contemporary Konrad Lorenz conducted ground-breaking work on imprinting by young birds. Breaking with goal-focused psychological explanations of behaviour, Lorenz was convinced that physiological rather than psychological methods should be used to explain animal behaviour in a scientific manner. According to Lorenzian ethology, animal behaviour had evolved over time due to Darwinian selection. Like a film sequence, researchers should break down complex behaviours into individual components (e.g. innate motor patterns) and analyse these components in relation to the wider physiological sequence. By breaking down behaviour like egg rolling by geese, it could be compared taxonomically among different animal species and its evolutionary origins could be reconstructed phylogenetically.²¹

According to Lorenz’s ‘hydraulic’ model of behaviour, animals were primed to carry out innate behaviour patterns that were triggered by environmental stimuli. Once a routine was finished, it would stimulate the next appropriate behaviour. Given the internal build-up of sufficient ‘action-specific’ behavioural energy, animals would first search for the appropriate stimulus (appetite behaviour) for a behaviour and eventually engage in this behaviour even in the absence of an appropriate stimulus (vacuum activities). Animals likely had no awareness of the purpose of a behaviour, and their lived experience would not change basic innateinstincts. While the goal-directedness of observed behaviours could be explained in evolutionary terms, researchers in the field should not confuse these (ultimate) causes with the (proximate) physiological and environmental triggers stimulating it.²²

Dutch biologist Nikolaas (Nikko) Tinbergen was also sceptical of ‘subjective’ animal psychology and laboratory-based ‘mechanistic’ behaviourist research. Characterised by historian Richard Burkhardt Jr as a hunter, he preferred research on ‘wild’ animals like digger wasps and herring gulls. Tinbergen had started researching animal behaviour during the 1930s and collaborated with Lorenz in Austria. Spending the wartime years in a Nazi prisoner camp, Tinbergen moved to Oxford in 1949. Although he initially shared Lorenz’s focus on physiological mechanisms of behaviour, criticism from US psychologist Daniel Lehrman and British ethologist Robert Hinde made Tinbergen abandon notions of unchangeable innate behaviour as well as his own—more elaborate—cascade model of hydraulic behaviour. From the early 1950s onwards, Tinbergen instead emphasised comparative field studies of animal behaviour and analyses of behaviours’ biological utility (survival utility) in complex ecological settings.²³ Drawing on work by Julian Huxley, Ernst Mayr, and Konrad Lorenz, he developed four complementary analytical approaches to interpret animal behaviour. Definitively set out in 1963, Tinbergen’s “four questions” provide the now classic definition of ethology and integrate a proximate physiological analysis of behaviour focusing on the (1) immediate causation of behaviour (mechanism) and its (2) ontogeny (development) with an ultimate analysis of behaviour focusing on the (3) function of a behaviour (evolutionary adaptation) and its (4) phylogeny (evolution). Answering the four questions may yield different answers, but answers will not contradict answers for the other questions.²⁴

By the late 1950s, European ethology was displacing laboratory-based behaviourist models with more complex environmentally situated and evolutionarily rooted explanations of animal behaviour. The field’s growing prominence was internationally recognised in 1973 when Tinbergen and Lorenz were jointly awarded the Nobel Prize in Physiology or Medicine with Karl von Frisch for their “discoveries concerning organization and elicitation of individual and social behaviour patterns.”²⁵ However, both Tinbergen and Lorenz consistently shied away from engaging with animal behaviour beyond directly observable traits. Fearing the Damocles sword of anthropomorphism and—in the case of Lorenz—committed to models of immutable innate behaviour, many continental ethologists avoided normative discussions of animal cognition, feelings (affective states), or welfare in laboratories or on farms.²⁶ Writing to Julian Huxley in 1959, Niko Tinbergen noted:

I am willing to admit that members of the same species can be supposed to feel roughly the same, but I think it is just futile even to try and argue [that one can understand how other species feel]—it is just not arguable. I will just willingly concede that we may suppose they feel the same. I cannot see how one can ever know whether one experiences what another man, another mammal, another vertebrate, another animal, another organism feels. That for me ends the matter—as long as we practice science.²⁷

Tinbergen’s compunctions were not shared by British ethologists. Similar to prominent scientists’ rise as public intellectuals in other Western countries,²⁸ the post-war years saw British behavioural researchers and biologists promote science’s role as a progressive socio-moral force.²⁹ Although Lorenz and Tinbergen also engaged with contemporary political debates,³⁰ their British counterparts believed that understanding animal cognition and feelings was key to developing a more humane science that would improve both animal welfare and society’s moral status. This thinking had a long tradition. By the early twentieth century, the antivivisection movement had sensitised generations of British researchers to ethical issues surrounding the treatment of animals and the societal embeddedness of their work.³¹ According to Robert Kirk, there was “broad agreement that the resulting Cruelty to Animals Act (1876) was positive for science and society alike.”³²

In 1926, leading zoologists, veterinarians, and scientists founded the Universities Federation for Animal Welfare (UFAW). Representing a ‘distinct amalgamation of pragmatic science and humane moral values,’³³ the UFAW tried to develop scientific solutions for animal welfare. Although it distanced itself from the ‘anti-scientific sentimentality’ of antivivisectionists, senior members like Charles Hume saw anthropomorphism ‘as a means to understand animal experience.’³⁴ Drawing on traditions of Christian social reform and evolutionary theories, Hume and others endorsed contemporary notions of kinship between animals and humans and developed a synthesist brand of “scientific humanism.”³⁵ For them, science was best positioned to morally improve society by finding rational ways to alleviate human and animal suffering. However, only a humane science could produce a humane society. In contrast to unsystematic earlier attempts to reduce cruelty, welfare emerged as a positive systematic concept, which could be measured, and regulated.³⁶

The Second World War catalysed UFAW efforts. Reports about barbaric Nazi experiments, new killing technologies, and Winston Churchill’s warnings about “perverted science” leading into the “abyss of a new Dark Age”³⁷ challenged progressivist doctrines of science as a force for moral progress. While the UFAW had previously addressed a plethora of issues ranging from the electrocution of slaughter animals to vermin control, the organisation increasingly focused on the humane treatment of animals used to produce scientific knowledge in the laboratory.³⁸ Initially targeting technicians rather than scientists, the UFAW’s engagement with laboratory practice was facilitated by new ethological interest in animal behaviour and contemporary calls for a more standardised supply of research animals. The emerging concept of stress was particularly important and enabled UFAW researchers like pharmacologist Michael Chance to present ‘well-being’ as a moral concern and a legitimate area of practical scientific inquiry. Using ethological methods to identify ‘normal’ species-specific behaviour of lab animals, Chance showed that different forms of social behaviour altered animals’ reaction to pharmaceutical drugs. Stressed animals in particular produced unreliable results. Stress could also be quantified. This opened the door to assessing well-being in different laboratory systems, establishing best practice guidelines, and warding off accusations of unscientific anthropomorphism.³⁹

In Oxford, zoologist William Moy Stratton Russell subsequently used indicators like breeding productivity and animals’ behaviour towards experimenters to create a welfare scale ranging from well-being to distress. Russell argued that good—and thus humane—research should aim to enhance well-being and reduce stress. In 1959, he co-authored The Principles of Humane Experimental Technique with Rex Burch. The publication laid out the influential 3Rs (replacement, reduction, and refinement) as a new ethical gold standard for the design of animal-dependent science. According to Robert Kirk, The Principles marked a late highpoint of the foregrounding of science’s moral mission within society.⁴⁰ To achieve this moral mission during a time of growing concerns about humans’ technological alienation from ‘nature’ and ethics, science had to actively incorporate humane values into its own practice.

UFAW members’ synthesist view of science, society, and ethics was shared by ethologist William Homan Thorpe. Working at Cambridge since 1932, Thorpe had begun his career as a neo-Lamarckian believing in the inheritance of acquired characteristics and researching insect behaviour and control. By the late 1930s, he had abandoned Lamarckianism in favour of Darwinian models of evolution and become interested in behavioural preferences’ role in driving speciation (“Baldwin Effect”). After reading the work of Konrad Lorenz, Thorpe shifted his research to studying instinct and learning in higher animals.⁴¹

As described by Gregory Radick and Neil Gillespie, this turn to ethology was influenced by Thorpe’s religious beliefs and increasingly outspoken support of Quakerism. Thorpe had started attending meetings of the Society of Friends around 1930 and formally converted to Quakerism after 1945. A conservationist and self-described “amateur philosopher-theologian,”⁴²Thorpe saw ethology as a way to reconcile his Christian beliefs with the modern synthesis of natural selection and Mendelian genetics by highlighting the “wholeness, of man and nature, and of the relation of both to the divine.”⁴³Thorpe’s natural theology rested on the concept of ‘creative’ evolution and was influenced by sociologist Leonard Hobhouse’s theory of evolution as a mind-expanding process, which had become self-conscious in humans.⁴⁴ According to Thorpe, human consciousness was the result of natural selection and emergence—an evolutionary event that could not be fully predicted by an organism’s phylogeny (evolution) or ontogeny (development). The emergence of consciousness was not mechanistic but ‘creative’ and its origins were purposeful. In addition to opening the door for divine design, postulating that consciousness was an emergent event with evolutionary power allowed Thorpe to reconcile humans’ animal origins with a view of their cognitive and spiritual uniqueness.⁴⁵ Thorpe’s theory of cognitive and behavioural evolution made him conceive of ethology as a somatic (bodily) and mental science.⁴⁶ It also necessitated seeing animals as something more than mindless machines, whose kinship with humans necessitated empathy.

Thorpian thinking influenced both British ethology and animal welfare politics. Having potentially met the young Ruth Harrison at Cambridge’s Quaker Meeting House or in his role as conscientious objector and chairman of the local Pacifists’ Service Bureau (see Chap. 3), Thorpe played a key role in bringing continental ethology to Britain after 1945. As the founding editor of Behaviour, he not only lobbied for a post for Lorenz in the UK but also helped engineer a reconciliation between Lorenz and Tinbergen—the former an erstwhile Nazi supporter and the latter a Nazi victim.⁴⁷ In Cambridge, Thorpe established and became the director of the Ornithological Field Station at Madingley, where he and his pupils researched the role of instinct, purposive behaviour, and insight learning in the development of chaffinch song. His research on wild birds and birds reared in auditory isolation revealed that learning occurred in two stages, with chaffinches learning first what to sing and then how to sing it. Additional work focused on breaking down instances of insight learning by birds and analysing the extent to which other species also imprinted on parents and whether this process was reversible.⁴⁸Thorpe’s findings not only challenged Lorenz’s theory of immutable instincts and Tinbergen’s agnosticism regarding animals’ affective states but also helped keep British ethology open to questions of welfare. If animals were self-aware and could think and learn, then frustrating their ‘normal’ behavioural impulses and needs—a concept developed by Thorpe’s student and colleague Robert Hinde⁴⁹—could be emotionally and mentally detrimental even if it did not cause physical harm.

Thorpe’s synthesist focus on animals’ affective states, cognitive evolution, and human morality was shared by Julian Huxley—albeit for entirely secular reasons. Since starting his research on bird behaviour in 1907, Huxley had credited animals with mental states and repeatedly stated that it was possible to know what these states were. Interpreting evolution as a progressive force for the good of a species, Huxley came to the conclusion that biological explanations of behaviour could not be reduced to aspects of sexual selection.⁵⁰ After ending his university career in the mid-1920s, Huxley became a public intellectual. In 1927, his bestselling The Science of Life, co-authored with H.G. and G.P. Wells, fused ecological, behavioural, and evolutionary concepts to argue for a synthesis between Darwinian evolution and Mendelian genetics. During the 1930s, Huxley intensified work with geneticists, mathematicians, and population biologists and coined the term “modern synthesis” in 1942.⁵¹ After a brief stint as the first director of the United Nations Educational, Scientific and Cultural Organization (UNESCO, 1946–1948), the 1950s saw Huxley re-emerge as a prominent British commentator on evolutionary theory, ethological research, wildlife conservation, and societal mores.

Similar to Thorpe, Huxley was particularly interested in the role that supposedly emergent evolutionary traits like language or cognition could play in shaping further evolution (Baldwin Effect).⁵² However, as a staunch atheist, Huxley disagreed with Thorpe on the causes of this emergence. Whereas Thorpe thought of the mind as the result of ‘creative’ emergence, Huxley thought of it as resulting from a secular but progressive evolutionary process. Writing to Thorpe in 1963, he noted:

you and I start from different premises. You assume the existence of absolutes and of some sort of super-person, or supernatural being, whereas I start from just the opposite angle … absolutes seem to me to be either the product of logical abstraction taken to an unreal extreme, or else … the result of all-or-nothing processes in our minds…⁵³

Rather than “reifying” the existence of the mind, Huxley advocated focusing on individual physiological components of cognition and promoted the term psychometabolism. Thorpe disagreed emphatically: “Of course I am reifying mind—that is the whole point. If I didn’t think that you had an entity such as mind I shouldn’t pay any attention at all to what you are saying.” According to Thorpe, secularists like Huxley were also assuming evolutionary absolutes but not admitting it:

I believe I could literally find a hundred statements or sentences in your various written works which imply that you do assume the existence of absolutes. I don’t want to start playing the game of the mote and the beam … but I do think some of these fundamental ideas at the basis of scientific thinking want to be brought out into the open, and I find personally that any of those who call themselves ‘humanists’ are wildly inconsistent just because they fail to do this.⁵⁴

This criticism was not unfair. Whereas Thorpe interpreted the emergent properties of the human mind as a sign of ‘creative’ divine evolution, which enabled humans to strive for spiritual improvement, Huxley conceived of cognition as the emergent result of precarious but ultimately progressive evolutionary forces.⁵⁵ As an advocate of ‘transhumanism,’ Huxley hoped that humans’ cognitive abilities would allow them to take charge of their evolutionary future in the form of a new religion of evolution, which included eugenics and birth control.⁵⁶ A better ethological analysis of the evolutionary roots of human behaviour—including affective states and cognition—was crucial to this endeavour. This put him at odds with Tinbergen’s insistence that animal feelings were outside the purview of ethology. Writing to Tinbergen in 1965, Huxley noted:

As regards subjective phenomena, it still seems to me that, just as one deduces that other human beings have subjective experiences of different sorts in relation to different circumstances, so we can and must deduce that different types of situations in animals are accompanied by different subjective states. … Total exclusive reliance on subjective approach is of course a very serious obstacle to progress in human psychology—but so is an uncritical materialist-behaviourist approach … I feel that ethology could and should become the basis for a real science of human psychology, and if so, it has to take account of subjective phenomena which by definition are involved in psychology!⁵⁷

The years after 1945 thus saw the synthesist orientation of British research on animal behaviour extend ethology’s remit to encompass animals’ cognitive and affective states. Breaking with continental ethologists and driven by senior British researchers’ theist and non-theist beliefs, this development in turn opened the door for active scientific engagement with the politics of animal welfare. It also created significant synergies with the moral agendas of emerging activists like Ruth Harrison, who often came from similar cultural and religious milieus. As a result of these synergies, the intensive farm would emerge as a crucible for activist and scientific thinking about animal welfare and the moral status of the humans producing these animals.