Comparative Cognition Research Research Articles

Affective sentience and moral protection

We have structured our response according to five questions arising from the commentaries: (i) What is sentience? (ii) Is sentience a necessary or sufficient condition for moral standing? (iii) What methods should guide comparative cognitive research in general, and specifically in studying invertebrates? (iv) How should we balance scientific uncertainty and moral risk? (v) What practical strategies can help reduce biases and morally dismissive attitudes toward invertebrates?

Gibbons exploit information about what a competitor can see.

How much nonhuman animals understand about seeing has been the focus of comparative cognition research for decades. Many social primates (and other species) are sensitive to cues about what others can and cannot see. Whether this sensitivity evolved in primates through shared descent or convergent evolution remains unclear. The current study tested gibbons-the apes that are least studied yet most distantly related to humans and one of the less social primates-in two food-competition tasks. Specifically, we presented eastern hoolock gibbons, Hoolock leuconedys, and silvery gibbons, Hylobates moloch, with a choice between a contested piece of food visible to both themselves and a human competitor and an uncontested piece visible only to themselves. Subjects successfully stole the uncontested food when the competitor turned away his body (N = 10, experiment 1) and his head (N = 9, experiment 2). However, when the head of the experimenter was oriented towards the contested piece of food, whether the competitor opened or closed his eyes made no difference. Subjects' sensitivity to body- and head-orientation cues was comparable to that of chimpanzees, rhesus macaques, and ring-tailed lemurs-species living in much larger groups than gibbons. These findings support the continuity hypothesis that sensitivity to body- and head-orientation cues is a product of shared descent among primates.

Sensory differences mediate species variation in detour task performance

Animal species differ considerably in their ability to detour around a see-through obstacle to reach a goal positioned behind it. This variation is commonly assumed to derive from interspecific differences in the cognitive functions involved in the execution of the task, such as spatial abilities and inhibitory motor control. A teleost fish, the guppy, Poecilia reticulata, has recently been found to outperform many mammals and birds in this type of task. To determine whether this is a typical condition in teleost fish or whether detour abilities vary among fish species as observed in mammals and birds, we compared four distantly related teleosts in a transparent barrier task using a group of conspecifics as the goal. The scores of three species (Poecilia reticulata, Xenotoca eiseni, Oryzias sarasinorum) were similar to those previously reported for fish. The remaining species, the zebrafish, Danio rerio, showed a much higher performance, close to that of warm-blooded animals with the highest scores (e.g. corvids and monkeys). In comparative cognition studies, contextual variables rather than differences in cognitive ability may be responsible for observed differences between species. In a second experiment, we found that the four species were similarly gregarious, excluding a different motivation to reach the target as an explanation for the different performance. In another experiment, however, we found evidence that the zebrafish's higher detour performance might be due to a sensory advantage. Zebrafish used olfactory cues (towards which the barrier was opaque) to navigate to the social stimuli, whereas the guppy, which we used as a control species, preferentially relied on visual information. This study highlights the importance of sensory differences as a source of potential experimental confound in comparative cognition research.

The Development of Sensorimotor Cognition in Common Ravens (Corvus corax) and its Comparative Evolution

Evolution involves developmental change. Species comparisons play an important role in comparative cognition because they can uncover common patterns and shared principles in cognitive evolution. Developmental studies reveal foundational elements of cognitive abilities and how they are constructed and integrated. Sensorimotor cognition is such a key element that forms the foundation for later-developing cognitive skills, yet little is known about its development in animals. This study uses 37 behaviors and tasks to investigate the development of Piagetian sensorimotor abilities in five young ravens (Corvus corax) from ages two to eleven weeks. Their developmental pattern largely mirrored that of twelve other bird and mammal species, albeit at a markedly accelerated rate. They reached the final sensorimotor stage, which to date has been shown only in great apes. The onset and sequence of sensorimotor development was identical for all species. Absolute number of neurons in the pallium and rest of brain was associated with achieving a higher stage across these species. This was not the case for absolute or relative brain mass, or number of neurons in the cerebellum or whole brain. We discuss the independent evolution of sensorimotor cognition and the importance of developmental pace and pattern therein. These findings show that the study of sensorimotor development is a useful tool for comparative cognition research. (Less)

Gaze following in an asocial reptile (Eublepharis macularius)

Gaze following is the ability to utilise information from another’s gaze. It is most often seen in a social context or as a reflexive response to interesting external stimuli. Social species can potentially reveal utilisable knowledge about another’s future intentions by attending to the target of their gaze. However, in even more fundamental situations, being sensitive to another’s gaze can also be useful such as when it can facilitate greater foraging efficiency or lead to earlier predator detection. While gaze sensitivity has been shown to be prevalent in a number of social species, little is currently known about the potential for gaze following in asocial species. The current study investigated whether an asocial reptile, the leopard gecko (Eublepharis macularius), could reliably use the visual indicators of attention to follow the gaze of a conspecific around a barrier. We operated three trial conditions and found subjects (N = 6) responded significantly more to the conspecific demonstrator looking up at a laser stimulus projected onto an occluder during the experimental condition compared to either of two control conditions. The study’s findings point toward growing evidence for gaze-following ability in reptiles, who are typically categorised as asocial. Furthermore, our findings support developing comparative social cognition research showing the origins of gaze following and other cognitive behaviours that may be more widely distributed across taxonomic groups than hitherto thought.

Meta-analytic techniques reveal that corvid causal reasoning in theAesop's Fable paradigm is driven by trial-and-error learning.

The classic Aesop's fable, Crow and the Pitcher, has inspired a major line of research in comparative cognition. Over the past several years, five articles (over 32 experiments) have examined the ability of corvids (e.g., rooks, crows, and jays) to complete lab-based analogs of this fable, by requiring them to drop stonesand other objects into tubes of water to retrieve a floating worm (Bird and Emery in Curr Biol 19:1-5, 2009b; Cheke et al. in Anim Cogn 14:441-455, 2011; Jelbert et al. in PLoS One 3:e92895, 2014; Logan et al. in PLoS One 7:e103049, 2014; Taylor et al. in Gray R D 12:e26887, 2011). These researchers have stressed the unique potential of this paradigm for understanding causal reasoning in corvids. Ghirlanda and Lind (Anim Behav 123:239-247, 2017) re-evaluated trial-level data from these studies and concluded that initial preferences for functional objects, combined with trial-and-error learning, may account for subjects' performance on key variants of the paradigm. In the present paper, we use meta-analytic techniques to provide more precise information about the rate and mode of learning that occurs within and across tasks. Within tasks, subjects learned from successful (but not unsuccessful) actions, indicating that higher-order reasoning about phenomena such as mass, volume, and displacement is unlikely to be involved. Furthermore, subjects did not transfer information learned in one task to subsequent tasks, suggesting that corvids do not engage with these tasks as variants of the same problem (i.e., how to generate water displacement to retrieve a floating worm). Our methodological analysis and empirical findings raise the question: Can Aesop's fable studies distinguish between trial-and-error learning and/or higher-order causal reasoning? We conclude they cannot.

The Value of Research in Comparative Cognition

Most research of comparative cognition has focused on the degree to which cognitive phenomena that have been reported in humans, especially children, can also be demonstrated in other animals. The value of such comparative research has not only been the finding that other animals show behavior that is qualitatively similar to that of humans but because the comparative approach calls for the careful control of variables often confounded with the mechanisms being tested, the comparative approach has identified procedures that could also improve the design of research with humans. The comparative approach has also been used to study the degree to which other animals demonstrate human biases and suboptimal behavior (e.g., commercial gambling). When applied to this field of research, the comparative approach has generally taken the position that human biases generally thought to be established by complex social and societal mechanisms (e.g., social reinforcement and entertainment) may be more parsimoniously accounted for by simpler mechanisms (i.e., conditioned reinforcement and positive contrast). When explained in terms of these mechanisms, the results have implications for explaining in simpler and more general terms the results of similar research with humans. Thus, comparative psychology tells us not only about the similarities and possible differences in behavior among species but it also may have implications for our understanding of similar behavior in humans.

Is a local sample internationally representative? Reproducibility of four cognitive tests in family dogs across testing sites and breeds.

A fundamental precept of the scientific method is reproducibility of methods and results, and there is growing concern over the failure to reproduce significant results. Family dogs have become a favoured species in comparative cognition research, but they may be subject to cognitive differences arising from genetic (breeding lines) or cultural differences (e.g. preferred training methods). Such variation is of concern as it affects the validity and generalisability of experimental results. Despite its importance, this problem has not been specifically addressed to date. Therefore, we aimed to test the influence of three factors on reproducibility: testing site (proximal environment), breed and sex (phenotype). The same experimenter tested cognitive performance by more than 200 dogs in four experiments. Additionally, dogs' performance was tested in an obedience task administered by the owner. Breed of dog and testing site were found to influence the level of performance only mildly, and only in a means-end experiment and the obedience task. Our findings demonstrate that by applying the same test protocols on sufficiently large samples, the reported phenomena in these cognitive tests can be reproduced, but slight differences in performance levels can occur between different samples. Accordingly, we recommend the utilisation of well-described protocols supported by video examples of the whole experimental procedure. Findings should focus on the main outcome variables of the experiments, rather than speculating about the general importance of small or secondary performance outcomes which are more susceptible to random or local noise.

Do Insects Have Emotions? Some Insights from Bumble Bees

While our conceptual understanding of emotions is largely based on human subjective experiences, research in comparative cognition has shown growing interest in the existence and identification of “emotion-like” states in non-human animals. There is still ongoing debate about the nature of emotions in animals (especially invertebrates), and certainly their existence and the existence of certain expressive behaviors displaying internal emotional states raise a number of exciting and challenging questions. Interestingly, at least superficially, insects (bees and flies) seem to fulfill the basic requirements of emotional behavior. Yet, recent works go a step further by adopting terminologies and interpretational frameworks that could have been considered as crude anthropocentrism and that now seem acceptable in the scientific literature on invertebrate behavior and cognition. This change in paradigm requires, therefore, that the question of emotions in invertebrates is reconsidered from a cautious perspective and with parsimonious explanations. Here we review and discuss this controversial topic based on the recent finding that bumblebees experience positive emotions while experiencing unexpected sucrose rewards, but also incorporating a broader survey of recent literature in which similar claims have been done for other invertebrates. We maintain that caution is warranted before attributing emotion-like states to honey bees and bumble bees as some experimental caveats may undermine definitive conclusions. We suggest that interpreting many of these findings in terms of motivational drives may be less anthropocentrically biased and more cautious, at least until more careful experiments warrant the use of an emotion-related terminology.

Reasoning by exclusion in the kea (Nestor notabilis).

Reasoning by exclusion, i.e. the ability to understand that if there are only two possibilities and if it is not A, it must be B, has been a topic of great interest in recent comparative cognition research. Many studies have investigated this ability, employing different methods, but rarely exploring concurrent decision processes underlying choice behaviour of non-human animals encountering inconsistent or incomplete information. Here, we employed a novel training and test method in order to perform an in-depth analysis of the underlying processes. Importantly, to discourage the explorative behaviour of the kea, a highly neophilic species, the training included a large amount of novel, unrewarded stimuli. The subsequent test consisted of 30 sessions with different sequences of four test trials. In these test trials, we confronted the kea with novel stimuli that were paired with either the rewarded or unrewarded training stimuli or with the novel stimuli of previous test trials. Once habituated to novelty, eight out of fourteen kea tested responded to novel stimuli by inferring their contingency via logical exclusion of the alternative. One individual inferred predominantly in this way, while other response strategies, such as one trial learning, stimulus preferences and avoiding the negative stimulus also guided the responses of the remaining individuals. Interestingly, the difficulty of the task had no influence on the test performance. We discuss the implications of these findings for the current hypotheses about the emergence of inferential reasoning in some avian species, considering causal links to brain size, feeding ecology and social complexity.

Keep Calm and Comp. Cog. On. Commentary: A crisis in comparative psychology: where have all the undergraduates gone?

Full Disclosure: We have recently authored an undergraduate textbook entitled Comparative Cognition (Olmstead and Kuhlmeier, 2015). Our motivation to write this book did not result from a perceived lack of undergraduate interest in the topic, but rather overenrolled courses for which we did not have a textbook. A key difference between our approach—largely shared by fellow commenters Brodbeck and Brodbeck (2015) and McMillan and Sturdy (2015)—and that of Abramson (2015), is our willingness to work under the title “comparative cognition.” We have been trained under various titles (e.g., biological anthropology, behavioral ecology, ethology, cognitive psychology, developmental psychology, and behavioral neuroscience) and have witnessed the continued emergence of comparative cognition as the logical intersection of these disciplines. Though, still considered a narrowly focused field by Abramson, we propose instead that comparative cognition has broadened (or perhaps always was broad, see Hulse et al., 1978; Wasserman, 1981), and encompasses, without conflict, Abramson's defining features of comparative psychology. Our point here goes beyond an argument about semantics, though it is important to be clear about our use of “comparative cognition,” Take, for example, a statement in the commentary by Bielert and Gallup (2015): “In particular, comparative cognition is quite similar to comparative psychology aside from restricting its research questions and measures to those specific to information processing (Shettleworth, 2010).” We do not see this “restriction” in scope in the modern practice of comparative cognition research. Instead, researchers consider the ways that general learning mechanisms may be constrained by early developing (perhaps innate) behavioral or perceptual biases, conceptual abilities, and/or non-conceptual processes. So yes, comparative cognition is open to the possibility of cognitive processes, but it actively tests for them. It also goes far beyond comparing behavioral responses of “species X” to that of humans (an anthropocentric approach that only a subset of researchers adopt, often with appropriate consideration of phylogenetics), and gone are the days of studying only a few, unrelated species. To use one metric: at the 2015 meeting of the Comparative Cognition Society, research with over 20 different species was presented. Shettleworth (2009), a pioneer and leader in the field, noted that comparative cognition research in the first decade of the twenty-first century was characterized by an increasing number of species examined and more synergy with related fields, such as behavioral ecology. A scholar of comparative cognition—and we think Shettleworth would agree with this based on her 2010 book—should be knowledgeable about sensory systems, behavioral tenets including general associative learning mechanisms, memory, and proposed cognitive mechanisms that are implicated in such areas as categorization, spatial navigation, number, timing, prosocial behavior, communication, and social learning, all the while considering an evolutionary, developmental, and neuroscientific framework. It's a tall order, but what an exciting field! In our experience, undergraduates agree. Like fellow commenters Furlong et al. (2015), we see the “missing” undergraduates every week—200 of them this term alone in a second year survey course: Introduction to Comparative Cognition. Many of these students will take our upper level laboratory courses that focus on specialized topics within the field of comparative cognition. The majority of these students specialize in other areas of psychology such as developmental, clinical, or cognitive psychology, a number are biology or life science majors, and a handful come from complementary disciplines such as computer science or philosophy. And yes, occasionally students seek out graduate study in laboratories specifically focused on comparative cognition. Regardless, we trust that they all pursue their chosen area of study with a greater appreciation and engagement in the basic, comparative science that informs so many fields of study.

From Crisis to Crowd Control. Commentary: A Crisis in Comparative Psychology: Where Have All the Undergraduates Gone?

From Crisis to Crowd Control. Commentary: A Crisis in Comparative Psychology: Where Have All the Undergraduates Gone?

Taking the Operant Paradigm into the Field: Associative Learning in Wild Great Tits.

Associative learning is essential for resource acquisition, predator avoidance and reproduction in a wide diversity of species, and is therefore a key target for evolutionary and comparative cognition research. Automated operant devices can greatly enhance the study of associative learning and yet their use has been mainly restricted to laboratory conditions. We developed a portable, weatherproof, battery-operated operant device and conducted the first fully automated colour-associative learning experiment using free-ranging individuals in the wild. We used the device to run a colour discrimination task in a monitored population of tits (Paridae). Over two winter months, 80 individuals from four species recorded a total of 5,128 trials. Great tits (Parus major) were more likely than other species to visit the devices and engage in trials, but there were no sex or personality biases in the sample of great tits landing at the devices and registering key pecks. Juveniles were more likely than adults to visit the devices and to register trials. Individuals that were successful at solving a novel technical problem in captivity (lever-pulling) learned faster than non-solvers when at the operant devices in the wild, suggesting cross-contextual consistency in learning performance in very different tasks. There was no significant effect of personality or sex on learning rate, but juveniles’ choice accuracy tended to improve at a faster rate than adults. We discuss how customisable automated operant devices, such as the one described here, could prove to be a powerful tool in evolutionary ecology studies of cognitive traits, especially among inquisitive species such as great tits.

Efficient search for a face by chimpanzees (Pan troglodytes).

The face is quite an important stimulus category for human and nonhuman primates in their social lives. Recent advances in comparative-cognitive research clearly indicate that chimpanzees and humans process faces in a special manner; that is, using holistic or configural processing. Both species exhibit the face-inversion effect in which the inverted presentation of a face deteriorates their perception and recognition. Furthermore, recent studies have shown that humans detect human faces among non-facial objects rapidly. We report that chimpanzees detected chimpanzee faces among non-facial objects quite efficiently. This efficient search was not limited to own-species faces. They also found human adult and baby faces-but not monkey faces-efficiently. Additional testing showed that a front-view face was more readily detected than a profile, suggesting the important role of eye-to-eye contact. Chimpanzees also detected a photograph of a banana as efficiently as a face, but a further examination clearly indicated that the banana was detected mainly due to a low-level feature (i.e., color). Efficient face detection was hampered by an inverted presentation, suggesting that configural processing of faces is a critical element of efficient face detection in both species. This conclusion was supported by a simple simulation experiment using the saliency model.

More than one way to see it: Individual heuristics in avian visual computation

Comparative pattern learning experiments investigate how different species find regularities in sensory input, providing insights into cognitive processing in humans and other animals. Past research has focused either on one species’ ability to process pattern classes or different species’ performance in recognizing the same pattern, with little attention to individual and species-specific heuristics and decision strategies. We trained and tested two bird species, pigeons (Columba livia) and kea (Nestor notabilis, a parrot species), on visual patterns using touch-screen technology. Patterns were composed of several abstract elements and had varying degrees of structural complexity. We developed a model selection paradigm, based on regular expressions, that allowed us to reconstruct the specific decision strategies and cognitive heuristics adopted by a given individual in our task. Individual birds showed considerable differences in the number, type and heterogeneity of heuristic strategies adopted. Birds’ choices also exhibited consistent species-level differences. Kea adopted effective heuristic strategies, based on matching learned bigrams to stimulus edges. Individual pigeons, in contrast, adopted an idiosyncratic mix of strategies that included local transition probabilities and global string similarity. Although performance was above chance and quite high for kea, no individual of either species provided clear evidence of learning exactly the rule used to generate the training stimuli. Our results show that similar behavioral outcomes can be achieved using dramatically different strategies and highlight the dangers of combining multiple individuals in a group analysis. These findings, and our general approach, have implications for the design of future pattern learning experiments, and the interpretation of comparative cognition research more generally.

Comparative cognition: An approach whose time has come

AbstractThe functional approach to comparative cognition research is exemplified by Shettleworth's (2010) book Cognition, Evolution, and Behavior. In this book, Shettleworth brings together the evolutionary perspective of behavioral ecology, the relative simplicity of behavior analysis, and the diverse research programs of cognitive psychology. This approach does not avoid the use of cognitive terminology but uses it to generate testable hypotheses that have the potential to provide evidence for or against the cognitive hypothesis. Unlike behavioral ecology and cognitive psychology, this approach postulates contingency learning as the default account of behavior but tests cognitive hypotheses against the default alternative. In this review, I present the results of three lines of research as examples of the kind of research that has been used to test cognitive hypotheses: functional equivalence, cognitive mapping, and rehearsal processes, all of which are covered by Shettleworth. In each case, I would argue that these experiments would not have been conducted had it not been for the hypothesis that a cognitive process might be involved. Whether or not evidence is found for the existence of a cognitive process, the results of such experiments are of interest for what they tell us about behavior as well as for their heuristic value.

Two fields are better than one: Developmental and cognitive perspectives on underatnding spatial reorientation

Two Fields Are Better Than One: Developmental and Comparative Perspectives On Understanding Spatial Reorientation Alexandra D. Twyman University of Western Ontario Daniele Nardi Sapienza University Nora S. Newcombe Temple University Reading Options: <a href=http://comparative-cognition-and-behavior-reviews.

Same/Different Concept Learning by Capuchin Monkeys in Matching-to-Sample Tasks

The ability to understand similarities and analogies is a fundamental aspect of human advanced cognition. Although subject of considerable research in comparative cognition, the extent to which nonhuman species are capable of analogical reasoning is still debated. This study examined the conditions under which tufted capuchin monkeys (Cebus apella) acquire a same/different concept in a matching-to-sample task on the basis of relational similarity among multi-item stimuli. We evaluated (i) the ability of five capuchin monkeys to learn the same/different concept on the basis of the number of items composing the stimuli and (ii) the ability to match novel stimuli after training with both several small stimulus sets and a large stimulus set. We found the first evidence of same/different relational matching-to-sample abilities in a New World monkey and demonstrated that the ability to match novel stimuli is within the capacity of this species. Therefore, analogical reasoning can emerge in monkeys under specific training conditions.

Flexibility in problem solving and tool use of kea and New Caledonian crows in a multi access box paradigm.

Parrots and corvids show outstanding innovative and flexible behaviour. In particular, kea and New Caledonian crows are often singled out as being exceptionally sophisticated in physical cognition, so that comparing them in this respect is particularly interesting. However, comparing cognitive mechanisms among species requires consideration of non-cognitive behavioural propensities and morphological characteristics evolved from different ancestry and adapted to fit different ecological niches. We used a novel experimental approach based on a Multi-Access-Box (MAB). Food could be extracted by four different techniques, two of them involving tools. Initially all four options were available to the subjects. Once they reached criterion for mastering one option, this task was blocked, until the subjects became proficient in another solution. The exploratory behaviour differed considerably. Only one (of six) kea and one (of five) NCC mastered all four options, including a first report of innovative stick tool use in kea. The crows were more efficient in using the stick tool, the kea the ball tool. The kea were haptically more explorative than the NCC, discovered two or three solutions within the first ten trials (against a mean of 0.75 discoveries by the crows) and switched more quickly to new solutions when the previous one was blocked. Differences in exploration technique, neophobia and object manipulation are likely to explain differential performance across the set of tasks. Our study further underlines the need to use a diversity of tasks when comparing cognitive traits between members of different species. Extension of a similar method to other taxa could help developing a comparative cognition research program.

What you see is what you get—Reloaded: Can jackdaws (Corvus monedula) find hidden food through exclusion?

Choice by exclusion, that is, the ability to base the choice of a target on the rejection of potential alternatives, is becoming increasingly interesting for comparative cognition research. Recently, ravens have been shown to solve an exclusion task and it had been suggested that this ability might benefit ravens in a food-caching context. To investigate this possibility, the raven study was replicated with a closely related, but noncaching, species, the jackdaw (Corvus monedula). In the first test, the birds had to find food hidden in one of two differently shaped tubes. The results suggest that the jackdaws found the food through intensive search behavior, with little evidence for exclusion abilities. In a follow-up experiment, the tubes were replaced by cups, and before the birds made a choice, one of the cups was lifted to inform them about its content. In a final task, this procedure was modified to control for the influence of local enhancement. In both experiments, the jackdaws were successful only if they had seen the food before. These findings are in contrast to the previous results on ravens and support the idea that exclusion abilities may have evolved as specific adaptations to food caching.