Temperament describes the idea that individual behavioural differences are repeatable over time and across situations. This common phenomenon covers numerous traits, such as aggressiveness, avoidance of novelty, willingness to take risks, exploration, and sociality. The study of temperament is central to animal psychology, behavioural genetics, pharmacology, and animal husbandry, but relatively few studies have examined the ecology and evolution of temperament traits. This situation is surprising, given that temperament is likely to exert an important influence on many aspects of animal ecology and evolution, and that individual variation in temperament appears to be pervasive amongst animal species. Possible explanations for this neglect of temperament include a perceived irrelevance, an insufficient understanding of the link between temperament traits and fitness, and a lack of coherence in terminology with similar traits often given different names, or different traits given the same name. We propose that temperament can and should be studied within an evolutionary ecology framework and provide a terminology that could be used as a working tool for ecological studies of temperament. Our terminology includes five major temperament trait categories: shyness-boldness, exploration-avoidance, activity, sociability and aggressiveness. This terminology does not make inferences regarding underlying dispositions or psychological processes, which may have restrained ecologists and evolutionary biologists from working on these traits. We present extensive literature reviews that demonstrate that temperament traits are heritable, and linked to fitness and to several other traits of importance to ecology and evolution. Furthermore, we describe ecologically relevant measurement methods and point to several ecological and evolutionary topics that would benefit from considering temperament, such as phenotypic plasticity, conservation biology, population sampling, and invasion biology.

/pdf/integrating-animal-temperament-within-ecology-and-evolution-2rq68t04zd.pdf

Integrating animal temperament within ecology and evolution.

EVOLUTION: Of Mice . . .

Biological reactivity to psychological stressors comprises a complex, integrated, and highly conserved repertoire of central neural and peripheral neuroendocrine responses designed to prepare the organism for challenge or threat. Developmental experience plays a role, along with heritable, polygenic variation, in calibrating the response dynamics of these systems, with early adversity biasing their combined effects toward a profile of heightened or prolonged reactivity. Conventional views of such high reactivity suggest that it is an atavistic and pathogenic legacy of an evolutionary past in which threats to survival were more prevalent and severe. Recent evidence, however, indicates that (a) stress reactivity is not a unitary process, but rather incorporates counterregulatory circuits serving to modify or temper physiological arousal, and (b) the effects of high reactivity phenotypes on psychiatric and biomedical outcomes are bivalent, rather than univalent, in character, exerting both risk-augmenting and risk-protective effects in a context-dependent manner. These observations suggest that heightened stress reactivity may reflect, not simply exaggerated arousal under challenge, but rather an increased biological sensitivity to context, with potential for negative health effects under conditions of adversity and positive effects under conditions of support and protection. From an evolutionary perspective, the developmental plasticity of the stress response systems, along with their structured, context-dependent effects, suggests that these systems may constitute conditional adaptations: evolved psychobiological mechanisms that monitor specific features of childhood environments as a basis for calibrating the development of stress response systems to adaptively match those environments. Taken together, these theoretical perspectives generate a novel hypothesis: that there is a curvilinear, U-shaped relation between early exposures to adversity and the development of stress-reactive profiles, with high reactivity phenotypes disproportionately emerging within both highly stressful and highly protected early social environments.

https://cals.arizona.edu/fcs/sites/cals.arizona.edu.fcs/files/D&P%20Boyce%20&%20Ellis%202005.pdf

Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity

The author explores the viability of a comparative approach to personality research. A review of the diverse animal-personality literature suggests that (a) most research uses trait constructs, focuses on variation within (vs. across) species, and uses either behavioral codings or trait ratings; (b) ratings are generally reliable and show some validity (7 parameters that could influence reliability and 4 challenges to validation are discussed); and (c) some dimensions emerge across species, but summaries are hindered by a lack of standard descriptors. Arguments for and against cross-species comparisons are discussed, and research guidelines are suggested. Finally, a research agenda guided by evolutionary and ecological principles is proposed. It is concluded that animal studies provide unique opportunities to examine biological, genetic, and environmental bases of personality and to study personality change, personality-health links, and personality perception.

From mice to men: what can we learn about personality from animal research?

Assessment of positive emotions in animals to improve their welfare.

Klein & Barron’s (K & B’s) suggestion that insects have the capacity for phenomenal consciousness is a refreshing and challenging departure from the cautious and agnostic stance that is taken by many researchers when considering this possibility. It is impossible to falsify the sceptic’s view that neural and behavioural parallels between humans and insects need not imply either similar conscious experience or even any phenomenal consciousness in insects at all. But if K & B are right, it is important to consider the possible contents of insect consciousness. Here we discuss whether affective consciousness, with its implications for potential suffering, might also be part of the simulated perceptual conscious world that K & B propose. Elizabeth S. Paul, Senior Research Fellow, University of Bristol, comparative psychologist, studies “emotion” and “mood” in human and non-human animals, reward processing in reinforcement learning, how emotions and moods influence decision-making, and empathy and individual variation in anthropomorphic thinking. http://www.bristol.ac.uk/vetscience/people/38480/ Michael T. Mendl, Professor of Animal Behavior and Welfare, University of Bristol, studies how attention, memory and decision-making influence and are influenced by affective state. In humans, affectinduced modulation of decision-making leads to “cognitive bias.” Can it be observed in animals and used as a novel indicator of animal affect (emotion) and welfare? http://www.bristol.ac.uk/vetscience/people/michael-t-mendl/ Klein & Barron (2016; henceforth K & B) follow Merker’s (2007) suggestion that dynamic integration of sensory information about the environment and the organism’s place in it, together with information about the organism’s current homeostatic requirements, generates a neural model that provides a “unique, unified perspective on the world” (K & B, p. 3) and produces consciousness. Merker argues that the vertebrate (human) midbrain is necessary and sufficient for consciousness, and that it embodies the neural simulation described above, integrating information from different decision-making domains — motivation, target (goal) selection, and action selection via a common-currency “conscious mode of function” (Merker, p. 71). K & B contend that the functional architecture of the insect brain has many parallels with that of the vertebrate midbrain and is thus capable of the same neural modelling, and hence of conscious experience. Animal Sentience 2016.128: Paul & Mendl on Klein & Barron on Insect Experience 2 But is consciousness a necessary corollary of neural computations of this sort -and does evidence of a similar functional architecture in human and insect brains inevitably imply a similar capacity for conscious experience? Even in humans, “blindsight” patients who are unable to report consciously seeing anything in their impaired visual field can exhibit precise real-time visually guided action and target selection (e.g., fine-tuning grasp to target size; avoiding obstacles). Interestingly, when a short delay is introduced between visual access to the task and task performance, these patients fail to fine-tune their movements or avoid obstacles; hence under these circumstances conscious experience is required (Striemer et al., 2009; Whitwell et al., 2011). Although damage to cortical pathways is involved in these phenomena, and there is debate as to whether blindsight patients truly lack phenomenal awareness in their impaired visual field (e.g., Merker), these findings raise the possibility that insects show neural coordination of motivation, target selection and action in the absence of conscious experience, at least in real-time. This possibility could be countered by good performance in tasks where there is a delay between target selection and action or goal acquisition. Sophisticated detour behaviour by jumping spiders hunting prey (Tarsitano & Jackson, 1997) may provide one such example. Notwithstanding these arguments, we find K & B’s proposal engaging and persuasive. We will now consider the potential contents of insect consciousness, should K & B turn out to be right. Although they avoid detailed consideration of this issue, K & B’s approach, like Merker’s, emphasises a perceptual, visual perspective. Merker (p. 72) speculates that “in its primitive beginnings, the ‘world’ of the proposed neural reality simulator presumably amounted to no more than a two-dimensional screen-like map of spatial directions on which potential targets might appear as mere loci of motion in an otherwise featureless noise field, defined more by their displacement than by any object features.” Such imaginings of the contents of subjective experience appear to sit well with K & B’s arguments for insect consciousness. Although predominantly visual, the same principles could conceivably be applied to a simulated world dominated by olfactory or auditory inputs. Within this simulated world, K & B (p. 5) note that “The motivational and physiological states of the organism prioritize target and action selection.” Goal prioritization and decisionmaking involve reward and punishment valuation mechanisms, adding an affective dimension to the simulation and, potentially, to the contents of consciousness. A primarily perceptually based consciousness could incorporate valuation of targets in a purely visual way by representing important goals as larger or more intense visual signals in the simulated world. Alternatively, affective consciousness – positively or negatively valenced feelings induced by fitness-enhancing or threatening stimuli – may have preceded perceptual experience as a common currency for evaluating different courses of action across functionally distinct domains (Cabanac, 1992; Mendl et al., 2010). Or both perceptual and affective consciousness may have emerged simultaneously as components of the simulated world. If either of the latter two scenarios applies in insects, the capacity for consciousness suggested by K & B would include subjective experience of affect (e.g., emotions), thus raising the possibility that insects can suffer, something that researchers and non-scientists think unlikely (Paul, 1995). The implications would therefore be significant, particularly ethically: At present insects are given no legal protection at all from harm. What is the Animal Sentience 2016.128: Paul & Mendl on Klein & Barron on Insect Experience 3 evidence that affective consciousness may be part of the simulated world proposed by K & B? Darwin (2009/1872, p. 347) attributed human-like emotions to insects: “Even insects express anger, terror, jealousy and love, by their stridulation.” For him, the functional and behavioural similarities between human and animal behaviour in emotive situations (e.g., in response to the arrival of a reward or a punisher) implied similarly subjective emotional experiences. Insects certainly show behavioural responses that resemble the fundamental features of emotions. Anderson & Adolphs (2014) call these “emotion primitives,” listing elements such as valence, scalability, and persistence as being critical for assigning emotionlike states to non-human animals. Fruit flies (Drosophila melanogaster), for example, show freezing and avoidance of a repeated looming shadow that becomes more intense with repeated exposure, and persists across time even after the shadow is removed. Gibson et al. (2015) argue that this reflects an emotion-like “internal defensive state” (p. 1401). Perhaps more compelling than immediate responses to stimuli is evidence that animals have background affective states, or “moods,” that function to moderate responses to events and guide decision-making, particularly under ambiguity. We (Mendl et al., 2010) hypothesize that an animal’s past experiences of reward and punishment across a range of functional domains (e.g., foraging, predator avoidance, intra-specific competition) determine its current mood state. Assuming a correlation between past experience and future probability of rewards and punishers, individuals can then make use of their mood state to “best guess” whether a novel or ambiguous stimulus is likely to be good or bad news; a negative mood should lead to enhanced expectation of punishment and/or decreased expectation of reward, resulting in cautious or “pessimistically” biased judgements of ambiguity (see also Nettle & Bateson, 2012). Honeybees, like a wide range of vertebrate species (Harding et al., 2004; Mendl et al., 2009; Gygax, 2014; Roelofs et al., 2016), show such affect-induced judgement biases (Bateson et al., 2011). Humans appear to make such judgements by reflecting on their subjective feelings, using the “how do I feel about it?” heuristic (Schwartz & Clore, 1983; Paul et al., 2005). This raises the possibility that affective consciousness plays a role in biasing judgements in insects and other invertebrates too. Although these examples are suggestive of affect-like states in insects, they do not provide conclusive evidence of conscious affective experience. Even in humans, there is no one-toone correspondence between reported emotional feelings and the behavioural and physiological components of emotional states. For example, Winkielman et al. (2005) found that participants viewing emotionally salient images showed behaviour indicative of an altered affective state (enhanced “liking” of a sweet drink, expressed through willingness to drink more and pay more for it) despite the absence of any change in subjectively experienced pleasure when consuming the drink. In terms of affect-induced judgement biases, it is possible to conceive a neural mechanism that reflects cumulative experience of reward and punishment and interfaces with action selection processes without needing to invoke conscious experience (Mendl et al., 2011). A candidate is changes in tonic firing of PPL and PAM dopaminergic neurones that code the valence of sensory input and moderate th

/pdf/if-insects-have-phenomenal-consciousness-could-they-suffer-ki2qgzyosm.pdf

If insects have phenomenal consciousness, could they suffer?

Elements of husbandry procedure, such as handling, may disrupt rodent social behaviour. Such effects may be contingent upon the familiarity between individuals and the quality and quantity of the disruption received. We investigated this issue using laboratory rats. We placed the rats into groups of three. At the point of group formation, 24 hours, one week and two weeks afterwards, individuals received one of three treatments: ‘handling’; exposure to novel conspecific ‘urine’; or ‘control’ (undisturbed), for a duration of either 5 or 15mins. We used a social recognition test to measure the ability of the rats to recognise the urine of group members of increasing familiarity following the implementation of these treatments. The ‘control’ treatment did not appear to disrupt social recognition. The 5-min ‘urine’ treatment appeared to disrupt recognition only when the rats had received the briefest experience of the familiar urine (5min). The 5-min ‘handling’ treatment, however, appeared far more disruptive, with an apparent disruption of social recognition even when familiarity with the urine donor was high (e.g. 7 days of group housing). Both the ‘handling’ and ‘urine’ treatments appeared more disruptive when presented for an increased duration (15min). There was also some evidence that increased experience of the handling procedure might reduce its disruptive effect. The results of this study have several implications for the welfare of laboratory housed rats, which are discussed.

Disruptive effects of standard husbandry practice on laboratory rat social discrimination

The use of cognitive bias as an indicator of affective state in the domestic dog

An investigation of the relationship between adrenal activity, social rank and immunocompetence in pregnant sows kept in different housing conditions

Within a species, some individuals are better able to cope with threatening environments than others. Paca (Cuniculus paca) appear resilient to over-hunting by humans, which may be related to the behavioural plasticity shown by this species. To investigate this, we submitted captive pacas to temperament tests designed to assess individual responses to short challenges and judgement bias tests (JBT) to evaluate individuals’ affective states. Results indicated across-time and context stability in closely correlated “agitated”, “fearful” and “tense” responses; this temperament dimension was labelled “restless”. Individual “restless” scores predicted responses to novelty, although not to simulated chasing and capture by humans in a separate modified defence test battery (MDTB). Restless animals were more likely to show a greater proportion of positive responses to an ambiguous cue during JBT after the MDTB. Plasticity in defensive behaviour was inferred from changes in behavioural responses and apparently rapid adaptation to challenge in the different phases of the MDTB. The results indicate that both temperament and behavioural plasticity may play a role in influencing paca responses to risky situations. Therefore, our study highlights the importance of understanding the role of individual temperament traits and behavioural plasticity in order to better interpret the animals’ conservation status and vulnerabilities.

https://research-information.bris.ac.uk/ws/files/263721258/nogueira_et_al_defensive_behaviour_in_paca_animals_2021.pdf

Michael Mendl

Papers

If insects have phenomenal consciousness, could they suffer?

Disruptive effects of standard husbandry practice on laboratory rat social discrimination

The use of cognitive bias as an indicator of affective state in the domestic dog

An investigation of the relationship between adrenal activity, social rank and immunocompetence in pregnant sows kept in different housing conditions

Temperament, Plasticity, and Emotions in Defensive Behaviour of Paca (Mammalia, Hystricognatha).