Taking Welfare into Account in Comparative Cognition Research
Abstract
Recognizing species-specific traits and individual experiences is crucial for understanding their impact on cognitive development and task performance. To reliably compare cognitive performance across species, it is vital to maintain consistency in husbandry, environment, and commensurate affective state, ensuring the same potential to develop and demonstrate their cognitive capacity. Given variations in welfare needs among species, populations, and individuals, developing species-specific indicators and measures is essential to assess, control, and better account for differences in current and cumulative welfare experiences.
Keywords: affective states, animal cognition, husbandry conditions, learning, psychology
When embarking on a comparative analysis of cognitive capacity, researchers are faced with the complex task of accounting and controlling for a multitude of confounding variables (internal and external) that may influence the outcomes of cognitive tasks. Several factors known to relate to current and past welfare experiences, including developmental history and motivational biases, can significantly alter task performance and confound comparisons. Careful control measures in experimental design and appropriate data analysis are thus required to properly compare task performance across individuals, populations, and species.
We acknowledge that there has been substantial progress in animal welfare science, yet this research field has historically concentrated on a restricted set of model species and farm animals. Thus, progress in this field is largely limited to knowledge of the motivations, needs, and natural behavior of a reduced number of key species and often relies on a few species-specific, animal-based welfare indicators. As animal cognition research expands beyond established model species to animals in zoos and the wild, the tools and approaches that we use to assess their welfare also need to expand. In this commentary, we aim to underscore two critical issues related to our understanding of welfare-relevant parameters within the context of current trends in comparative psychology.
First, despite the potential magnitude of the influence that species-specific welfare requirements can have on task performance and cognitive development, efforts to understand these requirements have been limited, especially for historically less well-represented species in cognitive research, such as the many species housed in zoos or observed in the wild. Second, an individual’s cumulative experience (or early life experience) and current affective states significantly impact the intensity and direction of their responses (i.e., positive or negative), and their capacity and willingness to respond to conditions, and thus their ability to cope with their environment. The husbandry and environmental conditions provided for animals under human care (i.e., animals in households, zoos, entertainment industry, labs or farms) will influence their affective states and can subsequently affect their cognitive development or significantly modulate their behavioral responses in cognitive paradigms—an issue that is particularly relevant for many long-lived model species, such as primates and corvids. Failing to recognize and account for these potential differences between individuals or populations raised and/or housed differently can confound and even invalidate results in comparative cognitive research because observed differences between individuals or populations could potentially relate to affect-driven cognitive biases or differences in stress levels and/or motivation rather than experimental treatments.
Species-Specific Welfare Requirements Can Affect Cognitive Task Performance
Animals under human care often experience rather barren husbandry and housing conditions that can limit their opportunities to engage with their physical and social environment, compared with the experiences that would be available in the wild (see Horn et al., 2022). In the wild, innate behaviors and cognitive skills are constantly used to navigate in challenging and changing environments. The lack of opportunity to express natural behavior can prevent the development of species-specific behaviors and can sometimes lead to frustration, boredom, and the display of abnormal behaviors (Mason & Burn, 2018). Studies have shown that the need for opportunities to express natural behaviors is highly species-specific and can have diverse effects on wild animals brought into captive environments (Mason, 2010). Moreover, as we continue to recognize the relevance of considering ancestral states, wild relatives, and ecological adaptations to understanding the development, behaviors, and cognitive capacity of model and farmed animals and attempt to account for it in studies (Mellor & Mason, 2023), gaining an understanding of the welfare needs of wild animals will become increasingly important. A long-standing line of research has shown that these behavioral limitations can exert a strong impact on performance in cognitive tasks and that the degree of impact will vary across species. The influence of social housing conditions on task performance has been empirically demonstrated in a variety of species (e.g., Costa et al., 2016; de Azevedo et al., 2023), including dairy calves (Gaillard et al., 2014), domestic pigs (Sneddon et al., 2000), elephants and cetaceans (Jacobs et al., 2022), rats (Parker et al., 2014), dogs (Milgram et al., 2005), and chickens (Patzke et al., 2009). Chronic or acute states of hunger can also have detrimental effects not only on health and productivity but also on task performance—dairy calves experiencing hunger during weaning displayed impairments in working memory and reference memory (Lecorps et al., 2023). Providing enrichment has also been shown to enhance performance in certain cognitive tasks. For example, when pigs were provided with peat and straw enrichment allowing them to root, their learning performance in an operant task and a maze task increased compared with pigs housed in a more barren environment (Sneddon et al., 2000). Besides more general husbandry settings, mental stimulation can also play a role in altering the outcomes of cognitive tasks. Goats in enriched housing show improved learning abilities in a four-choice discrimination task compared with those in barren conditions (Oesterwind et al., 2016).
These examples illustrate that husbandry conditions that are more tailored to a species’ specific behavioral and environmental needs allow them to engage with their environment, and consequently enhance their welfare experience, which can have positive influences on the individual’s cognitive development and cognitive task performance. It is particularly important to be aware of limitations in our knowledge of husbandry demands and welfare requirements when new species are introduced into comparative cognitive research—for example, in large multispecies comparative approaches that include species for which we neither have institutionalized husbandry guidelines nor validated welfare indicators. It is also essential to be aware of the diversity that exists among species and individuals’ cognitive responses. Thus, when trying to standardize husbandry environments, it is imperative to recognize that a particular environment could adversely affect the welfare of one species (or a population or an individual) while leaving others relatively unaffected (e.g., Mellor et al., 2021). Despite a growing awareness of the relationship between welfare, husbandry, and cognitive task performance, investigators often do not systematically account for individual differences in welfare parameters or housing conditions in their experimental design or interpretation of results.
Past and Current Affective States Alter Cognitive Development and Decision-Making Processes, Affecting Cognitive Task Performance
The literature on cognitive bias strongly supports the idea that the underlying affective state of animals significantly influences the assessment of their environment and their decision-making processes (Crump et al., 2018; Mendl et al., 2009). Through so-called judgment bias tests, researchers have consistently found that an animal’s emotional well-being directly correlates with how it interpret and respond to ambiguous cues (Baciadonna & McElligott, 2015; Lagisz et al., 2020). When animals are in a positive emotional state, they tend to exhibit an optimistic bias, expecting positive outcomes from ambiguous stimuli. Conversely, animals experiencing negative emotional states demonstrate a pessimistic bias, anticipating negative consequences. This example highlights the bidirectional interaction between an animal’s emotional state and its cognitive functioning, and it emphasizes the crucial role that welfare plays in shaping an animal’s behavior and affecting its decision-making processes (Lagisz et al., 2020; Neville et al., 2020).
It is important to recognize that an individual’s current and future decision-making, cognitive processes, and welfare experiences are not solely shaped by their current experiences and affective state. They can also be influenced by their past welfare experiences, including early life experiences and affective states experienced in the past, which result in their cumulative welfare experiences. From animal welfare and mental health literature, we know that past experiences can shape current behavioral responses, influencing the degree, direction, and intensity of an individual’s response to stressors (i.e., habituation vs. sensitisation). Moreover, past affective states can exert a lasting influence on an individual’s personality, such as boldness or shyness (Found, 2022), which in turn is associated with greater or reduced learning capacity and decision-making abilities (Dougherty & Guillette, 2018). Thus, the combined and accumulated welfare experience of individuals is increasingly understood to have a significant influence on their capacity and motivation to exhibit a behavioral, physiological, or other response to contemporary exposure to a stimulus (Langenhof & Komdeur, 2018). Studies into post-traumatic stress have shown variation in both the magnitude and character of the reaction that individuals who experienced past trauma will have when exposed to both known and novel contemporary stressful situations (George et al., 2015). Hence, it is important to control for these potential differences in baseline welfare conditions when seeking to compare and interpret performances in cognitive tasks. Making use of long-term welfare markers such as telomere lengths (Bateson, 2016) and changes in the local amount of gray matter in their hippocampus (Poirier et al., 2019), in combination with shorter-term markers, can provide a baseline for comparison, establish comparability between subjects before investigation, aid with accurate interpretation of results, and help identify individuals that may need to be removed to enhance the informativeness of studies.
Comparative cognitive research in captive animals must extend beyond evaluating an individual’s current state by embracing a holistic approach that encompasses their entire life history. This approach aligns with the STRANGE framework proposed by Webster and Ruiz (2020) and emphasizes the crucial role that past affective states have in shaping an individual’s cognitive capacities and the need for framing experimental observations of individuals within the context of their unique welfare experiences.
Conclusion
The significant variation in welfare requirements of different species underscores the need to better understand species-specific differences in life-history characteristics and how they influence those needs. We must possess not only a profound comprehension of foraging behaviors, social dynamics, and other ecological factors but also a deep understanding of the unique welfare needs of each species and how to evaluate these needs over their entire lifetime. Establishing this understanding and insight will aid in reaching a consensus on how to assess whether animals have experienced similar welfare levels throughout their lives and how to account for it in experimental design and results interpretation. Achieving an accurate assessment of cognitive performance that enables valid interspecific comparative analysis thus necessitates holding welfare experiences constant across species and populations by tailoring conditions appropriately. Failure to do so can introduce biases, hinder reproducibility, or inaccurately suggest that individuals in negative emotional states are representative of healthy animal models.
In conclusion, the intricate relationship between both past and current welfare experiences, affective states, and cognition highlights the need to consider both the past (accumulated) and present experiences and diverse needs of individuals when assessing their cognitive functioning, and this will persist as a key challenge for the field of comparative cognition that merits further exploration and investigation.
References
Baciadonna, L., & McElligott, A. G. (2015). The use of judgement bias to assess welfare in farm livestock. Animal Welfare, 24, 81–91. https://doi.org/10.7120/09627286.24.1.081
Bateson, M. (2016). Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context? BioEssays, 38, 201–212. https://doi.org/10.1002/bies.201500127
Costa, J. H. C., Von Keyserlingk, M. A., & Weary, D. M. (2016). Invited review: Effects of group housing of dairy calves on behavior, cognition, performance, and health. Journal of Dairy Science, 99, 2453–2467. https://doi.org/10.3168/jds.2015-10144
Crump, A., Arnott, G., & Bethell, E. J. (2018). Affect-driven attention biases as animal welfare indicators: Review and methods. Animals, 8, Article 136. https://doi.org/10.3390/ani8080136
de Azevedo, C. S., Cipreste, C. F., Pizzutto, C. S., & Young, R. J. (2023). Review of the effects of enclosure complexity and design on the behaviour and physiology of zoo animals. Animals, 13(8), Article 1277. https://doi.org/10.3390/ani13081277
Dougherty, L. R., & Guillette, L. M. (2018). Linking personality and cognition: A meta-analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1756), Article 20170282. https://doi.org/10.1098/rstb.2017.0282
Found, R. (2022). Nutritional stress and population density influence risk/reward decisions by elk. Wildlife Research, 50(2), 152–159. https://doi.org/10.1071/WR22040
Gaillard, C., Meagher, R. K., von Keyserlingk, M. A., & Weary, D. M. (2014). Social housing improves dairy calves’ performance in two cognitive tests. PloS ONE, 9, Article e90205. https://doi.org/10.1371/journal.pone.0090205
George, S. A., Rodriguez-Santiago, M., Riley, J., Abelson, J. L., Floresco, S. B., & Liberzon, I. (2015). Alterations in cognitive flexibility in a rat model of post-traumatic stress disorder. Behavioural Brain Research, 286, 256–264. https://doi.org/10.1016/j.bbr.2015.02.051
Horn, L., Cimarelli, G., Boucherie, P. H., Šlipogor, V., & Bugnyar, T. (2022). Beyond the dichotomy between field and lab—the importance of studying cognition in context. Current Opinion in Behavioral Sciences, 46, Article 101172. https://doi.org/10.1016/j.cobeha.2022.101172
Jacobs, B., Rally, H., Doyle, C., O’Brien, L., Tennison, M., & Marino, L. (2022). Putative neural consequences of captivity for elephants and cetaceans. Reviews in the Neurosciences, 33, 439–465. https://doi.org/10.1515/revneuro-2021-0100
Lagisz, M., Zidar, J., Nakagawa, S., Neville, V., Sorato, E., Paul, E. S., Bateson, E. S., Mendl, M., & Løvlie, H. (2020). Optimism, pessimism and judgement bias in animals: A systematic review and meta-analysis. Neuroscience & Biobehavioral Reviews, 118, 3–17. https://doi.org/10.1016/j.neubiorev.2020.07.012
Langenhof, M. R., & Komdeur, J. (2018). Why and how the early-life environment affects development of coping behaviours. Behavioral Ecology and Sociobiology, 72, Article 34. https://doi.org/10.1007/s00265-018-2452-3
Lecorps, B., Woodroffe, R. E., von Keyserlingk, M. A., & Weary, D. M. (2023). Hunger affects cognitive performance of dairy calves. Biology Letters, 19, Article 20220475. https://doi.org/10.1098/rsbl.2022.0475
Mason, G. J. (2010). Species differences in responses to captivity: Stress, welfare and the comparative method. Trends in Ecology & Evolution, 25(12), 713–721. https://doi.org/10.1016/j.tree.2010.08.011
Mason, G. J., & Burn, C. C. (2018). Frustration and boredom in impoverished environments. In M. C. Appleby, I. A. S. Olson, & F. Galindo (Eds.), Animal welfare (pp. 114–138). CAB International. https://doi.org/10.1079/9781786390202.0114
Mellor, E. L., & Mason, G. J. (2023). Feeding, mating and animal wellbeing: New insights from phylogenetic comparative methods. Proceedings of the Royal Society B, 290(1994), Article 20222571. https://doi.org/10.1098/rspb.2022.2571
Mellor, E. L., McDonald Kinkaid, H. K., Mendl, M. T., Cuthill, I. C., van Zeeland, Y. R., & Mason, G. J. (2021). Nature calls: Intelligence and natural foraging style predict poor welfare in captive parrots. Proceedings of the Royal Society B, 288, Article 20211952. https://doi.org/10.1098/rspb.2021.1952
Mendl, M., Burman, O. H., Parker, R. M., & Paul, E. S. (2009). Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Applied Animal Behaviour Science, 118, 161–181. https://doi.org/10.1016/j.applanim.2009.02.023
Milgram, N. W., Head, E., Zicker, S. C., Ikeda-Douglas, C. J., Murphey, H., Muggenburg, B., Siwak, C., Tapp, D., & Cotman, C. W. (2005). Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: A two-year longitudinal study. Neurobiology of Aging, 26, 77–90. https://doi.org/10.1016/j.neurobiolaging.2004.02.014
Neville, V., Nakagawa, S., Zidar, J., Paul, E. S., Lagisz, M., Bateson, M., Løvlie, H., & Mendl M. (2020). Pharmacological manipulations of judgement bias: A systematic review and meta-analysis. Neuroscience and Biobehavioural Review, 108, 269–286. https://doi.org/10.1016/j.neubiorev.2019.11.008
Oesterwind, S., Nürnberg, G., Puppe, B., & Langbein, J. (2016). Impact of structural and cognitive enrichment on the learning performance, behavior and physiology of dwarf goats (Capra aegagrus hircus). Applied Animal Behaviour Science, 177, 34–41. https://doi.org/10.1016/j.applanim.2016.01.006
Parker, R. M., Paul, E. S., Burman, O. H., Browne, W. J., & Mendl, M. (2014). Housing conditions affect rat responses to two types of ambiguity in a reward–reward discrimination cognitive bias task. Behavioural Brain Research, 274, 73–83. https://doi.org/10.1016/j.bbr.2014.07.048
Patzke, N., Ocklenburg, S., Van der Staay, F. J., Güntürkün, O., & Manns, M. (2009). Consequences of different housing conditions on brain morphology in laying hens. Journal of Chemical Neuroanatomy, 37, 141–148. https://doi.org/10.1016/j.jchemneu.2008.12.005
Poirier, C., Bateson, M., Gualtieri, F., Armstrong, E. A., Laws, G. C., Boswell, T., & Smulders, T. V. (2019). Validation of hippocampal biomarkers of cumulative affective experience. Neuroscience & Biobehavioral Reviews, 101, 113–121. https://doi.org/10.1016/j.neubiorev.2019.03.024
Sneddon, I. A., Beattie, V. E., Dunne, L., & Neil, W. (2000). The effect of environmental enrichment on learning in pigs. Animal Welfare, 9, 373–383. https://doi.org/10.1017/S096272860002296X
Webster, M. M., & Rutz, C. (2020). How STRANGE are your study animals? Nature, 582, 337–340. https://doi.org/10.1038/d41586-020-01751-5