Cognitive Ethology Carolyn A

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Cognitive ethology Carolyn A. Ristau∗

Cognitive Ethology, the field initiated by Donald R Griffin, was defined by him as the study of the mental experiences of animals as they behave in their natural environment in the course of their normal lives. It encompasses both the problems defined by Chalmers as the ‘hard’ problem of consciousness, phenomenological experience, and the ‘easy’ problems, the phenomena that appear to be explicable (someday) in terms of computational or neural mechanisms. Sources for evidence of consciousness and other mental experiences that Griffin suggested and are updated here include (1) possible neural correlates of consciousness, (2) versatility in meeting novel challenges, and (3) animal communication which he saw as a potential ‘window’ into their mental experiences. Also included is a very brief discussion of pertinent philosophical and conceptual issues; cross-species neural substrates underlying selected cognitive abilities; memory capacities especially as related to remembering the past and planning for the future; problem solving, tool use and strategic behavioral sequences such as those needed in anti-predator behaviors. The capacity for mirror self-recognition is examined as a means to investigate higher levels of consciousness. The evolutionary basis for morality is discussed. Throughout are noted the admonitions of von Uexkull¨ to the scientist to attempt to understand the Umwelt of each animal. The evolutionary and ecological impacts and constraints on animal capacity and behavior are examined as possible. © 2013 John Wiley & Sons, Ltd.

How to cite this article: WIREs Cogn Sci 2013, 4:493–509. doi: 10.1002/wcs.1239

INTRODUCTION they behave in their natural environments in the course of their normal lives. The mental experiences included, hatisitliketobeabat?’... the title of 1 among others, awareness, purposes, consciousness, ‘Wa philosophical essay by Nagel. He argued and general and specific cognitive capacities. that we could never know what such an experience His endeavor provoked considerable contro- was like, for as human beings/scientists, we have no versy. But as Griffin had earlier remarked in 1958, way of determining or understanding the nature of concerning biologists’ great reluctance to consider any bat mind state. In correspondence with Nagel the possibility of animals’ use of sonar for echolo- 2,3 and in his writings, Donald R. Griffin the founder cation (now well established), ‘Excessive caution can of ‘Cognitive Ethology’ argued otherwise... that it sometimes lead one as far astray as rash enthusiasm.’4 was indeed possible to make at least a start into He proposed exploring several lines of evidence such investigations, and even, assuming evolutionary for this new field: (1) possible neural correlates of continuity of mental experience, to imagine some consciousness; (2) versatility of organisms in adapting of the experiences of other organisms. Cognitive to new challenges for which they have not been Ethology was to be a beginning scientific exploration either genetically prepared or had pertinent learning of the mental experiences of animals, particularly as experiences; (3) communication by animals, that can be interpreted as reporting subjective experiences. ∗Correspondence to: [email protected] Findings have potential impacts on human Department of Psychology, Barnard College of Columbia behavior. We are more likely to be concerned about University, New York, NY, USA animal’s well being and conservation of their habitat Conflict of interest: The author has declared no conflicts of interest if we understand them to be conscious, intelligent for this article. beings.

A BRIEF FORAY INTO PHILOSOPHICAL including perspective taking, empathy, and generally ISSUES CONCERNING COGNITIVE the ability to model another’s mental and physical 16–18 ETHOLOGY perspective). Awareness and Consciousness The problems Griffin raises about consciousness are Approaches to the Study of Animal what the philosopher Chalmers,5 in a seminal paper, Capacities has termed the (phenomenal) ‘hard’ problems and the A significant contribution to the study of animals is the ‘easy’ problems. The latter, in Chalmers’ view, are concept von Uexkull¨ 19 proposed in 1909, that of the those in which, using methods of cognitive science, ‘Umwelt,’ meaning the environment as an organism the phenomena appear to be explicable (someday) in perceives it and interacts with it. Several organisms terms of computational or neural mechanisms. The can appear to live in the ‘same’ environment, but ‘easy’ problems entail cognitive abilities including in effect those environments are vastly different, discriminating, integrating information, deliberately with each organism sensing and emphasizing different controlling behavior, and accessing and reporting aspects, interacting differently, using the environment mental states among others. (It should be noted differently. that many scientists would consider that such ‘easy’ Another approach to species comparisons is problems require more than a neural/computational a ‘functional’ one. Thus ethologists describe and approach, a very reductionistic type of explanation.) compare foraging strategies, food preparation/storage, The ‘hard’ problems are the phenomenological ones, territory selection/defence, selection/creation of a the very experience of a mental state, a perception, home, mate selection, parenting behavior and the a pain, ‘what it is like to be xxx.’ In the past, concomitant cognitive skills required in each. We most scientists have avoided the ‘hard’ problems. have learned that cognitive abilities in one sphere Many philosophers, however, including Aristotle,6 need not generalize to another. Such modularity raises Descartes,7 and contemporary philosophers of the issue of ‘what’ has evolved?What circuitry? Are mind8–11 have been concerned with issues of animal there ‘core knowledge systems’ common to humans consciousness and reason. The philosopher Searle12,13 and some other species20–22 or can abilities in one is probably most closely aligned with the stances of sphere generalize to another(s)... over the eons or Griffin, and considers that a main issue is not whether possibly in an organism over a lifetime? We do find nonhuman animals are conscious, but which animals many examples of one available biological ‘solution’ are conscious and to what level of consciousness. being used over evolution for other purposes.23 Even Darwin entitled a book ‘The Expression of Truly appropriate comparisons of abilities the Emotions in Man and Animals.’14 As Griffin notes, across species likewise entails understanding the Darwin’s inclusion of mental continuity in evolution developmental and learning processes involved: does is far more reasonable a scientific approach than the capacity occur full-blown in all species members? beginning with the denial of such capacity. Griffin What experiences/learning trials were required; how further suggests that a yet more conservative, neutral many; over how long a time? approach would be to assume p = 0.5 with respect to Work with captive species has revealed abilities the probability of consciousness in animals and then possibly latent in the natural environment. In a few to increase or decrease that probability as data are instances, captive great apes have been observed to accumulated.15 actively teach as distinguished from exhibiting a Nevertheless, despite confusion over definitions, behavior which may be copied. For example, the more (not all) contemporary animal behavior sci- signing chimpanzee (Pan troglodytes) Washoe actively entists appear to grant, to at least some species, molded the hands of young chimpanzee Loulis into phenomenological ‘awareness’ or ‘primary conscious- the sign for food, a training technique often used ness,’ if not the higher levels of consciousness. Those by humans with Washoe.24 Some captive apes, in higher levels are often termed ‘sentience,’ described particular, young apes, achieve abilities not observed as the depth of awareness of self and others. Sen- in the field, e.g. spontaneous pointing, and do so more tience includes self-awareness (both self as a body readily if they have more (positive) interactions with entailing self-recognition and self including a men- humans.25 Even monkeys can be specifically taught tal entity existing in a continual fashion in the to point and then they generalize to use the skill in a past, present, and future), metacognition (the abil- communicative manner in varied circumstances.17 ity to think about the contents of one’s own mental We need to recognize that some observed states/feelings), and Theory of Mind (various abilities behaviors may be ‘default,’ those exhibited in urgent

494 © 2013 John Wiley & Sons, Ltd. Volume 4, September/October 2013 WIREs Cognitive Science Cognitive ethology circumstances or in the presence of very potent stimuli, Brain Structures Underlying Cognitive and can be detrimental in that particular situation. In Capacities less constrained circumstances, the organism may have Despite current disagreements about directly linking reacted differently. For example, the beavers’ cognitive specific neural activity or areas with consciousness, abilities utilized in dam construction and repair certain brain structures have been shown to play sig- have been denigrated, because some experimental nificant roles in both humans and other species, under- work indicated that a beaver plastered mud over lying similar kinds of cognitive competencies. In par- a loudspeaker that produced white noise, a sound ticular, the hippocampus (in vertebrates) is intrinsic to 26 similar to water rushing through a leak. That learning and storing spatial information, such as land- behavior can likewise be interpreted as a useful marks, distances and directions, all of which can figure failsafe, while dam repair is achieved more flexibly importantly in locating food, territory and dwelling 27 in many circumstances. sites, scatter hoarding, migration, and mating.33 In short there is a need for cautious conclusions Some avian species, particularly corvids, typ- and openness to various approaches. ically investigated in the laboratory, exhibit aston- ishing abilities to cache food for times of scarcity, some species retrieving in a matter of hours, others in months.34 Hippocampal size varies with spatial NEUROLOGICAL AND demands placed on animals by their ecology, with NEUROANATOMICAL ISSUES increasing neurogenesis rates for winter storage and declines during spring. For example, in black-capped Neural Correlates of Consciousness chickadees (Poecile gambeli) large differences in mem- Despite intensive efforts to date (2012), research to ory and hippocampal size occur over both large find Neural Correlates of Consciousness (NCC) has continental scale differences in winter severity as well not revealed structures or processes unique to humans as over small spatial scales that occur with the increas- that are necessary for consciousness. It must also be ingly harsh conditions as one ascends a mountain; noted that neither have any necessary and sufficient significant differences occur over as little as 600 m neural correlates of consciousness been determined. of elevation.35,36 Hippocampal size also varies with We have learned that consciousness involves many mating systems; polygamous species needing to roam levels of brain functioning from brainstem to the over larger territories to find mates have a larger 28 cortex. hippocampus than do monogamous species.37 A proper discussion of NCC is beyond the scope Homologous brain structures have been sought 17 of this ms. Refer to Griffin and Speck or resources for the language learning of human children and non- concerning neural studies and theories as they relate human animals’ vocal communicative development. to the possibility of demonstrating consciousness in Many parallels have been found in avian song learn- 29,30 nonhuman animals. Evidence includes pharmaco- ing such as babbling and sound crystallization. Yet, logical interventions that can affect human conscious among primates, it is chimpanzee gestural communi- behavior, use of human consciousness studies, such as cation that may provide interesting parallels as well binocular rivalry and blindsight and relating all these as possible homologous neurological structures.29,38 to similar investigations and behaviors in nonhumans. Relative brain size with respect to body weight Further supportive evidence for widespread conscious- shows parrots and corvids (such as crows, rooks, and ness is offered by Panksepp’s research31 emphasizing jays) are comparable to chimpanzees, with humans deep, old subcortical systems that generate affective topping the list; dolphins particularly, but even seals, consciousness and emotional expression. Quite sim- also have high ratios. Generally that greater relative ilar systems occur in all mammals and some birds. brain size is associated with advanced cognitive When stimulated in humans, they produce intense processing and with high levels of sociality, longevity, emotional feelings and associated behaviors. In non- slow development and long parental investment as humans, stimulation produces similar behavioral and well as a large forebrain.39 Interestingly it is different physiological responses and, it is interpreted, similar brain structures that show these correlations. In conscious feelings. Not all agree. humans and other mammals, it is the cortex; in birds Referring to this and other research, a group it is the nidopallium, until recently not considered a of eminent cognitive scientists recently signed the homologous structure.37,40 ‘Cambridge Declaration on Consciousness,’ basically Forebrain size has been linked to different stating that humans are not unique in possessing the abilities in different species. In birds, the linkage neurological substrates that generate consciousness.32 appears to be to innovative behavior. In ungulates

Volume 4, September/October 2013 © 2013 John Wiley & Sons, Ltd. 495 Advanced Review wires.wiley.com/cogsci and primates forebrain size is linked more closely to of the Mirror Self Recognition test until the paradigm social dynamics41 such as intra-group co-ordination includes the opportunity to explore a larger mirror and aspects of group size; linkage may also be to the with the tip of its trunk.53 type and quality of bonding relationships.42 The capacities can be different as in the honey In fact the most pertinent commonalities bee’s detecting both polarized light, and, like many between primates, including humans, and birds, are other insects, UV light. To some, UV signifies open virtually identical neuronal connections and microcir- space, not the dark nest, for the sun is the only cuits that have been recently identified as mediating natural source of UV. To the honeybee, UV light also similar behaviors.43 allows perceiving floral patterns that provide ‘paths’ Very different neural systems can subserve to nectar/pollen. In von Uexkull’s¨ famous example, complex behaviors, namely that of cephalopods, a tick sucks not a human, but the rock wet with particularly the octopus, likely squid, possibly butyric acid from the sweaty man no longer there. cuttlefish.44–46 The octopus nervous system has three The horse’s visual system allows it to detect something main parts: a large brain of two central masses, the very well along the horizon, but in other regions, it arm nervous system, and optic lobes. The system has somewhat reduced acuity; this is attributed to a consists of about 500 million neurons, in contrast long streak of ganglion cells across the retina which to rats’ 100 million and dogs’ 600 million.47 That parallel the slit-like pupil of the horse’s eye.54 brain is among the largest of any invertebrate and the What is to be constructed from the sensory brain/body ratio of Octopus vulgaris is comparable to systems is another matter. ‘Search image’ has been that of lower vertebrates.48 The octopus may have proposed as a learned and/or innate sensory pattern undergone convergent evolution with vertebrates, facilitating an organism’s finding a particular food needing extensive memory and learning perhaps type, especially cryptic ones. On the other hand, driven in part by its being a solitary hunter or simply detecting change in the environment and/or exacerbated by its vulnerability due to loss of the from a learned sensory pattern is critically important ancestral shell.49 The mammalian hippocampus and for ‘lower’ species such as sharks and lobsters; acute octopus MSF-VL system in the large brain lobes sensitivity to changing odor concentration in water are similar, specifically in architecture, physiological currents can lead the animals to the source, food.55 connectivity and the exceptionally high number of Cross-modal matching is achievable by horses (and small interneurons in the learning and memory areas. other species); horses can discriminate by voice cues Convergence is not complete, with typical invertebrate between a familiar and unfamiliar person, then match neural communication, particularly with respect to voice to visual/olfactory cues.56 cell structure and membrane properties. However, We likely have not yet discovered the full array of like those in other species, activity-dependent synaptic other organisms’ sensory capacities; adaptive behavior plasticity exists in neural areas important for learning of some species before earthquakes or approaching and memory.50 storms suggests sensitivities we do not know. In conclusion, the hippocampus and other brain structures are subserving similar and complex functions in different species. The critical aspect ANIMAL COMMUNICATION appears to be similar micro patterns of individual Natural Animal Communication neural connections rather than the brain region per se. Animal communication encompasses a broad array of signals, including visual, acoustic, electromagnetic, SENSING (AND INTERACTING WITH) vibration, and odor. The focus here will be on THE ENVIRONMENT vocal communication, which has received extensive investigation, probably because auditory signals As emphasized in von Uexkull’s¨ concept of Umwelt, can readily be recorded, then used in ‘playback’ nonhuman animals’ sensory systems differ from each experiments. other and from humans, not only in sensing capacities, Among the core issues are: (1) whether signals but also in senses emphasized and means of gathering are emitted in a reflexive, emotive Groan of Pain and utilizing the sensory information. A chimpanzee mannerasGriffintermedit,57 or via an Innate in a signing project initially learns not that the Releasing Mechanism (IRM) as earlier described by sign for flower signifies ‘flower,’ but rather the ape, Tinbergen58 or whether some voluntary control exists. presented with a flower, generalizes to associate the (2) the meaning of the communication. Indeed Griffin sign with other odors such as pipe tobacco and saw animal communication as ‘a window on animal kitchen fumes.51,52 An elephant appears incapable minds.’2 (3) then, how to investigate these issues?

Voluntary Usage? Presently, scientists are attempting to fine tune The issue was addressed with the concept ‘audience their approach to studying signaling, including more effect,’ which examines the impact of a particular studies beyond alarm and food calls. Smith’s suggested conspecific’s presence on the likelihood of a analysis, though difficult, can help elucidate signal communicator uttering a given vocalization.59,60 For information. Townsend and Manser,70 in their excel- example, a male might make ‘food calls’ in the lent review, suggest variants of playback experiments, presence of food and a female, but not if another including prime-probe, habituation-dishabituation male were present instead of the female. and violation of expectation techniques. In analyzing animal vocal communication, scientists differentiate between (1) the acoustic structure Information in Alarm Calls of the call, (2) the usage, and (3) comprehension, Most scientists agree that alarm calls contain distinguishing between information that a scientist urgency-based information (predator’s threat level). recognizes in the call and the recipient(s)’ comprehen- Interpretation of the referential component of calls sion and utilization of that information. is much more controversial. Apparent categories Many factors may impact on whether a potential of functionally referential information potentially vocalizer calls and whether the recipient actually available in an alarm signal are: predator type (aerial responds and how. These factors, addressed already or terrestrial, specific species), predator’s spatial in 1977 by Smith,61,62 include past history of the location, physical qualities such as size, shape, and organism, likely unknown to the researcher. Such color, and predator behaviors such as movement (no concerns are not limited to ‘intelligent’ organisms; movement, speed, kind of movement such as hawk familiarity and social history have been shown to perched, searching for prey or attacking72). affect the signaling of Siamese fighting fish.63 Initial distinctions between calls for aerial and some ground predators were noted from astute obser- Meaning of Signals vations of vervet monkeys (Cercopithecus aethiops) Smith64 encouraged a ‘message-meaning analysis’ of by an experienced field researcher (Struhsaker)73 and signals, noting that the same auditory production were then followed up by videotaped playback experi- can have different meanings, depending on recipient ments in the field.64 Since then, acoustically distinctive and context (including past history, environment, calls for aerial and for ground predators have been and other stored information). Thus a male bird’s found in a diverse number of species, including chick- springtime song may mean to another male ‘likely ens(Gallus gallus domesticus),66,74 many species of aggression by me if you approach’ or ‘come hither’ ground squirrels (Spermophilus spp.),75 tree squir- to a female. Messages may include information rels (Tamiasciurus hudsonicus),76 social mongooses about the signaler’s behavior and probability thereof, (aka Meerkats) (Suricata suricatta),77 prairie dogs location, individual or group identity, or external (Gunnison’s (Cynomys gunnisoni) and Black-tailed referents such as predators, food, events or other (Cynomys ludovicianus)),78 and various lemurs79 and ‘things.’ Message-meaning analysis requires detailed monkeys80–83 (reviewed in Ref 84). For some species observations about correlations with conditions and the calls appear to be quite specific in their refer- signaler and recipient(s)’ behavior, prior to, during ents, for example, the vervet monkeys have three and after the signal. It is difficult to do well. types of calls causing differential responding, for A simpler methodology, with significant lim- example, looking upward and running to a nearby itations, but widely adopted probably due to that bush to the call for eagle-type predators, looking simplicity, relies on ‘functional referents.’ Calls are so to the ground for snake-type calls and running up classified if they appear to be highly stimulus specific65 into the trees or remaining quietly there for calls for and if call recipients use that specificity to determine leopard-like predators.64,72 [These responses, how- the nature of their adaptive response.66–70 This anal- ever, are not absolutely unique to each predator type, ysis sidesteps the issue of information contained in with occasional similar responses across categories as the call, requiring a ++ behavioral response as evi- indicated in both the original and more recent data. dence for the ‘functional referent;’ it has thus been Recent studies also show a sex difference, with only used primarily with so-called ‘food ‘ and ‘alarm’ calls. female vervets exhibiting the distinctive responding Concerns with this analysis and the playback experi- (J. Fischer, personal communication)]. Social mon- ments typically used, center on the lack of contextual gooses calls distinguish aerial versus ground preda- information available to a recipient with which to tors at different urgency levels.85 Various species of calibrate responses, and thus a higher likelihood of a prairie dogs appear to have both distinctive calls and ‘default’ or fail-safe response.63,71 appropriate responding behavior to the calls for at

Volume 4, September/October 2013 © 2013 John Wiley & Sons, Ltd. 497 Advanced Review wires.wiley.com/cogsci least four different potential predators (coyote (Canis by the introduction of discriminant functional analysis latrans), domestic dog (Canis familiaris), red-tailed (DFA) and other statistics,100 replacing some of hawk (Buteo jamaicensis), and human (Homo sapi- the tedious measurement and possible subjectivity ens)75,86,87) and also possibly to badgers (Taxidea in classification. Acoustic structural differences do taxus),88 ferrets (black-footed (Mustela nigripes)89 reliably sort calls according to descriptors such as and snakes, including specific snake species.90 Some- color, size, and shape and other conditions, but, in times species have both specific and broadly used many cases, we are unable to provide evidence, at this alarm77 and mobbing calls.91 There is evidence as point, that call recipients are using that information. well for some interspecies recognition of alarm calls Why do such complex communication systems (discussion in Ref 92). exist in some species? The alarm systems of Some of the most perplexing interpretations of prairie dogs and meerkats may have resulted from data are for alarm calls said to denote predator evolutionary pressures deriving from their ecological characteristics such as size, color, or shape. These conditions. For example, prairie dogs are a fixed social distinctions have been reported for prairie dogs,85,93 species, subject to the same predator individuals, but black-capped chickadees also appear to encode with fairly set escape opportunities (bolt holes and information about predator size,94 and male chickens tunnels).101 Some individual predators have different provide graded information about aerial stimuli size, strategies: some coyotes rapidly charge at any prairie distance and speed, to which captive females respond dogs; others wait at a well-populated burrow.102 It in graded fashion in experimental situations.95 would be beneficial to recognize those individuals, Is some call information (e.g., size, speed, dis- perhaps aided by color or shape information. The tance) merely a correlate of urgency? Slobdochikoff’s field needs further explorations of communication experiments argue against that interpretation, in that complexity across species and ecological conditions. acoustic structure of prairie dog alarm calls varied with colors on intruders and were distinctive for certain geometric shapes (triangle vs. circle–square).96 Caching, Episodic Memory, and Mental Slobodchifkoff (pers. comm.) suggests that the geo- Time Travel metric sensitivities may be related to the prairie dogs’ Whether animals have episodic memory remains predator classes: triangular for raptors, circular–rect- debated still, Tulving103,104 having claimed it to be a angular for mammalian ground predators. uniquely human capacity. Episodic memory (‘remem- Plasticity ber’) is distinguished from semantic memory (‘know’). Plasticity, originally thought to be the property only To remember, for Tulving, includes recognizing that of human language, has been found in song birds it is oneself in the past episode and in the present; that (Oscines), then in hummingbirds (Trochilidae)and assertion is most difficult to establish in a nonlinguis- parrots (Psittaciformes)97 and then more widespread. tic organism. Evidence supports close relationships Some species show gradual development to the adults’ between episodic memory and the ability to project more complex acoustic alarm calls (e.g., prairie dogs, oneself into the future, with shared neural systems 105,106 meerkats).Prairie dogs have been shown to modify and developmental paths. Planning for oth- calls made to a human intruder if that intruder became ers seems to precede developmentally planning for more threatening (e.g., fired a gun). Goat (Capra self, a distinction Clayton suggests may be useful in 104 hircus) contact calls have been shown to exhibit plas- animal studies. Whatever the difficulties of interpre- ticity, affected both by kinship and membership in tation, there have been useful criteria established for different social groups.98 These differences potentially investigating ‘episodic-like’ memory in nonhuman ani- promote mother-kid recognition, individual identity, mals: (1) the what–where–when paradigm, and (2) the and the formation of ‘dialects’ indicative of social ‘unexpected question’ technique. group membership. Growing evidence supports vocal In a set of ingenious experiments, Clayton production learning in some other mammalian species: and colleagues, allowed scrub jays (Aphelocoma bats, pinnipeds, cetaceans and elephants (discussion in coerulescens) to bury larvae, a preferred food and, 107 Ref 97). There are scattered references to refinement in a separate place, peanuts, less preferred. The of usage93 and development of unique food calls in birds had learned that the larvae decay and become some primate species.99 inedible after five days, but the peanuts do not. Given a choice soon, or after five days, the scrub jays chose the Further Questions appropriate spot to retrieve the food. This experiment How to conceptualize present findings in animal fulfilled the what-where-when conditions. However, communication? Analysis has been greatly facilitated subsequent research indicated limited success beyond

498 © 2013 John Wiley & Sons, Ltd. Volume 4, September/October 2013 WIREs Cognitive Science Cognitive ethology the food caching corvids, and only scrub jays met all birds, particularly the corvids, some cetaceans, fishes, the conditions the researchers set. invertebrates including octopi, and, surprisingly, in The ‘unexpected question’ paradigm suggested only five species of nonprimate mammals. Veined by Zentall108 tests for something that was incidental octopi (Amphioctopus marginatus) have been filmed at the time of training (presumably ‘unattended’ by carrying discarded coconut shells along as they walk, the animal), using a probe trial inserted within the requiring an ungainly inefficient ‘stilt walk’ to do ordinary testing trials. As Clayton et al note, a useful so, then using the shells for protective shelter as approach for future studies. needed.111 The mammals observed using tools in the PROBLEM SOLVING, TOOL USE, AND wild are some Asian elephants (Elphas maximus) STRATEGIC BEHAVIOR SEQUENCES which modify branches to swat away flies, sea otters (Enhydra lutris) which frequently use rocks to break Problem Solving the shells of clams and sea urchins, some bottle nose Kohler¨ 109 set chimpanzees problems to acquire out- dolphins (Tursiops sp) using sponges to protect body of-reach food, having boxes available that could be parts while foraging, humpback whales (Megaptera piled up or poles that could be fit together. Kohler¨ novaeangliae) which blow bubble curtains used to reported that the chimpanzees solved these problems trap fish schools , and as recently observed, brown spontaneously, not by stimulus–response association bears (Ursus arctos) which scratch themselves with or trial and error, but by a sudden insight. There are selected, barnacle encrusted rocks.112 The topic has other interpretations of the chimpanzees’ behavior. several extensive reviews113–116 and will be mentioned Many other species were subsequently also seen to be only briefly here. capable of various problem solving tasks. In captivity, various species, not observed Some of the most remarkable understandings, using tools in the wild, have been taught tool interpreted as comprehending causal relations, are use, including rooks (Corvus frugilegus)117 and exhibited in Heinrich’s experiments with ravens wood pecker finches (Cactospiza pallida)118 or have (Corvus corax).110 In one set, adult captive ravens independently demonstrated tool creation and use.18 with no experience with strings, after several hours, One of the more remarkable instances of tool creation pulled up meat dangling on a meter long piece of involved captive New Caledonian crows (Corvus string. They pulled up sections, stood on the captured moneduloides). A female crow, having seen a wire string, and repeated this motion until reaching the hook, but never having witnessed the process of meat. If startled, ordinary ravens fly off with any food bending wire, nevertheless, bent a wire into a hook in their mouth. In this experiment, a raven who was to reach food down a tube. This creation involved unsuccessful at pulling up the food, did try to fly away innovative behavior and nonnatural materials, not with meat on a string, but those who had pulled up the likely to be encountered in the wild.119 meat did not do so, even on the first startle. In other The definition of tool use is a continuing experiments with crossed colored strings, one holding debate, but most scientists agree that it requires a rock and the other meat, some ravens immediately the manipulation of a freely movable object on a pulled on the correct string. Other ravens did so after target object to modify the target object’s physical a brief tug moved the unpalatable rock. However they characteristics.113 Using tools is of especial interest persisted over subsequent trials in initially pulling the because it implies a goal or purpose, requires at incorrect string, directly under which hung the rock, least short-term planning (sometimes longer) and, then corrected and pulled the string which moved the depending on the context, can require flexible meat. Another task, with different ravens and a looped behavior. Some species can also modify their tools string which ‘illogically’ required pulling down on the to be more efficient. string to move the meat up was never successfully The definition of tool use can also be solved and the ravens lost interest. We do not know extended.111 For example, Tinbergen reported all causal relations or ‘physics’ the ravens understand, Herring gulls picking up clams (movable) and or the ‘rules’ they apply, but gradually, across species, opening them to eat by dropping them onto rocks we may be able to determine ecologically appropriate (stationary).120 A gorilla used a stick apparently to generalities. determine water depth, thus improving its access to information.121 Mike, the well known Goodall study Tool Use chimpanzee, improved his display by loudly banging In the wild, tool use has been observed in a wide array discarded kerosene cans, such continued usage finally of taxa, including all great apes, some monkeys, some resulting in a rise in his status.122

Given the diversity of species capable of tool Protecting the Young: Injury Feigning Birds use and the various specialized uses, it is likely that Some ground nesting birds when having a nest or there are different cognitive mechanisms and different young, will perform various apparently distractive ecological and social constraints/drivers underlying behaviors in the presence of a predator or intruder. the capacity, as is true of many cognitive abilities. For the Piping plover (Charadrius melodus), these include flying conspicuously in front of the intruder, Strategic Behavior Sequences vocalizing near the intruder, ‘false brooding’ (sitting fluffed out on a site where there is no nest), or Introduction the most dramatic, engaging in very awkward wing- Strategic behaviors exhibited by animals can reveal flapping, commonly termed ‘broken-wing displays’ both cognitive complexity and intended behavior. or ‘injury feigning.’ So ‘injured,’ the bird may The behaviors are relevant to issues of representation display, sometimes for many minutes or for hundreds and intentionality, both in the philosophical sense of feet, but then simply flies away. The birds of intentionality and ‘intended’ or ‘purposeful’ give an impression of trying to lead the intruder (included within a concept of intentionality).123 away from the nest, though some have claimed Several aspects of strategic behaviors are of particular the movements are ‘hysterical’ and others have interest to Cognitive Ethologists: organisms must claimed the movements are released and directed be able to prioritize between conflicting demands, 130 131 for example, courting, mating, feeding self, feeding throughout by sign stimuli. Ristau investigated young, protecting young, hunting, avoiding predation. the possibility that the behavior is purposeful, applying what Dennett has termed a first order Animals also often need to use spatial information, 8 recognize and take advantage of opportunistic events, intentional stance, namely that ‘the plover wants overcome obstacles, especially novel ones, learn to lead the intruder away from the nest/young.’ through either actual or mental trial and error, and A purposeful interpretation suggests the following sometimes even deceive. predictions: (1) the plover should move in a direction Great apes’ strategic behaviors are well such that an intruder following it would move documented,124,125 so I will note lesser known cases, further from the nest or young, (2) the plover should firstly, those of an ungulate, the pronghorn antelope monitor the intruder’s behavior, and (3) the plover (Antilocapra Americana).126 Their complex antipreda- should respond appropriately to changes in the tor behavior also supports evolution of a specialized intruder’s behavior. intelligence, not via the social intelligence hypoth- Ristau found that in 44/45 cases the Piping esis,127 but rather from the driving force of predation, plover displayed while moving in a direction that in the antelopes’ case, particularly on the young. would lead the intruder away from the nest. The bird did monitor the intruder and changed its behavior if Predator Avoidance Behavior/Protecting Young: an intruder stopped following the display, including Antelopes such actions as flying or walking closer to the intruder In general, ungulate adults avoid predation by or displaying more intensely. being large bodied and/or fast runners. However, The bird also chose its location for display, as reported by Byers,118 mother pronghorn antelope sometimes flying, which, in all cases examined, hide vulnerable newborns, staying away and, before resulted in the bird being closer to the intruder. returning, run about, even for a half an hour, often The plovers also quickly learned to discriminate staring, appearing to look for predators. The high between humans who had behaved in ‘threatening’ predation pressure at Byers’ site, results in 75–100% ways and those who had not, namely those who of the fawns falling to coyotes or eagles.128,129 Byers previously had hovered over the nest and those reports a returning mother suddenly seeing two low- who had simply walked by, not looking at the flying golden eagles. The doe leaves the young’s nest. Only one or two exposures were necessary. region, craning back her head, a posture used only Others have interpreted the ‘broken-wing’ behavior when looking at golden eagles. She then waits 30 min, of plover species in a much more minimal way. departing again when the eagles return. Byers,123 for example, contrasts the ungulates’ With coyotes, Byers reports that the antelope ‘calculated’ behavior with that of another plover mother, usually positioned far from the young (about species, the killdeer (Charadrius vociferous). He 70 m), extrapolates from the coyote’s path, distracting claims the killdeer parents display no matter what only when the coyote’s path will intercept the fawns. his path, dependent only on his approach distance. She then flashes her large white rump patch and However, as demonstrated in the above research prances distinctively. by Ristau129 with a related species, the plover’s

500 © 2013 John Wiley & Sons, Ltd. Volume 4, September/October 2013 WIREs Cognitive Science Cognitive ethology display is not static, but on a path leading away a high bounding gait (‘stotting’)135; hares stand from the young. Readiness to display does appear bipedally.136 And prey likewise carefully monitor to depend on previous exposure to humans, birds predator activities, seeming able to detect when initially being very wary, likely to display and predators are not dangerous, either resting at a doing so at greater approach distances. Ristau’s distance or otherwise engaged.137 detailed sequential analysis, adopting the stance of Some predators are capable of co-operative possible purposeful behavior, does lead to a deeper hunting, from simple to complex, particularly in chim- appreciation of the complexity of the interactive panzees and lionesses (Panthera leo), but observations behavior, than does simply noting approach distance. exist also of pelicans (Pelacanus crispus), cormorants This use of the intentional stance is instrumental (e.g., Phalacrocorax auritus), Harris’s hawks (Parabu- in nature, helpful in suggesting experimental work teo unicinctus), and likely other birds of prey, South and meaningful kinds of observations. As various American otters (Pteronura braziliensus), dusky dol- philosophers and scientists have suggested, further phins (Lagenorhynchus obscurus), killer whales (Orci- conceptual work is needed to better theoretically nus orca), hyenas (notably Crocuta crocuta), and other ground these and other behaviors studied/analyzed species.138 by cognitive ethologists.132

Predatory Strategies MIRROR SELF RECOGNITION Strategies are also required by the predators. Very EXPERIMENTS well documented accounts show individual members The mirror self-recognition (MSR) experiments139 are of genus X overcome obstacles to reach their prey, of interest for several reasons. In these, a mark is taking long detours around, often losing visual contact placed on an organism where it cannot be seen with that prey. In danger themselves of predation except by the organism’s viewing its own reflection by their prey, they are opportunistic, moving closer in a mirror. The successful subject tries to explore when such movements are disguised or the prey is or remove the mark. Human children pass this test distracted by other events. Some of the predator’s between 18 and 24 months of age, other species which communication is highly similar to that used in the succeed, at later ages. Gallup and later de Waal prey’s courtship and suffices to mislead the prey. have suggested that MSR capacity has coevolved with Genus X is any of several jumping spiders, Portia. empathy and perspective taking.140,141 And species These large venomous spiders build their own webs with those capacities have evolved with complex social to capture insects, but also specialize in preying upon group structures and/or interactions. other spiders by invading their webs. Portia plucks Although a myriad of species have been tested, the strings of the prey’s web, sometimes similarly from chickens and beyond, only humans, great apes, to the prey’s courtship vibrations. Signals that bring dolphins (Tursiops truncates),142 Asian elephants the prey closer to the web edge are continued, (Elephas maximus),51 and magpies (Pica pica),143 otherwise varied. Some signals are like those of the only nonmammalian species, have succeeded. a ruffling breeze or falling leaf. Should a breeze Arguments can be made for homologous evolution in blow, Portia advances, under protection of those humans and great apes, but would require convergent vibrations. Should the prey advance aggressively, evolutionary mechanisms for the other species. Portia retreats. Portia may return, even a half an To succeed does not imply having the same hour later, but often with a different tactic, perhaps capacity for self recognition that humans do; that dropping precisely from above, on a silken thread, capacity develops gradually beyond MSR. MSR onto the prey, killing it with a poisonous bite. In entails recognition of self as a body, not self as a laboratory experiments, Portia can, on first encounter, mind, or psychological entity existing in the past, successfully capture novel spiders, never encountered present, and future. in its evolutionary history.16,133,134 Critics will invent When individuals pass the test, they go through a myriad of complex modules to deal with these several stages. Initially they (1) give ‘social displays,’ phenomena; others may suspect that some cognitive reacting to the image as an ‘other,’ often threatening, capacities may reside in such organisms. sometimes courting, then (2) physically inspect the mirror, even looking behind it, (3) test for behavioral Other Aspects of Predator and Prey Behavior contingencies, often passing repeatedly in front of Alerting predators to one’s presence is a tactic that the mirror, and (4) inspect the marking. In tests is used by many species, when predation appears with successful species, not all individuals pass, some to rely on surprise, for example, antelopes produce stopping at earlier stages or losing interest altogether,

Volume 4, September/October 2013 © 2013 John Wiley & Sons, Ltd. 501 Advanced Review wires.wiley.com/cogsci not uncommon behavior for non-MSR tasks too. relationships mattered; this occurred only for cage- For gorillas and orangutans, some researchers report mate pairs. In fact, males, but not females, showed a success and others failure. counter-empathetic reaction, reducing their own pain Why the magpie succeeds at MSR, while parrots, sensitivity when witnessing the pain of unfamiliar a social and very cognitively advanced species, have males, presumably likely rivals.150 not, is unclear. The magpie is a corvid, stores food, A sense of fairness has been investigated, requiring detailed memory capacity, and remembers specifically ‘inequity aversion,’ a term from economics who has observed its storing, suggesting strong social theory. In seminal research with capuchin monkeys sensitivities.144 Of five magpies tested, clear MSR (Cebus apella), the monkeys refused to accept a evidence occurred in two birds, weaker in another piece of cucumber, a less preferred food that they and not in two. had been exchanging with the experimenter for Why do tests fail for some experiments and some tokens, when their partner suddenly started receiving species? The successful Asian elephant tests allowed highly preferred grapes instead of cucumber.151 the elephant to explore the mirror with its trunk, a The results set off a flurry of controversy and primary appendage for assessing its environment,52 research, discussed in an excellent review by and provided a far larger mirror for the elephant Brosnan and DeWaal.152 Most research entailed to view than had earlier work.145 Interestingly, the non-human primates, and sometimes dogs (Canis elephant used the smaller mirror to locate hidden lupus familiaris), generally indicating negative food; such instrumental mirror use without passing responses to continuing inequity between an animal MSR has occurred in various species. The direct and a social partner, with the disadvantaged gaze entailed in MSR is, in many species, particularly often refusing to continue the task. Cleaner fish primates, an aggressive communication and so may (Labroides dimidiatus) which work cooperatively, impact on exploration of the image. Despite some punish those not contributing to the cleaning.153 debate about MSR,146 it does appear to require However, in experiments, they did not exhibit advanced cognitive/social abilities and so remains a inequity aversion, suggesting that punishment, useful comparative technique.147 rather than sensitivity to equity, can maintain cooperation.154 What of the other side of injustice, the MORALITY ‘advantaged inequity’ of the one receiving more. Morality is considered by many to have its roots This ‘second order inequity,’ considered as deriving in emotional and empathetic behavior. DeWaal from the first, and weaker, does, at least sometimes and colleagues specifically propose roots in empa- with chimpanzees, lead to the advantaged individual thy/consolation, pro-social tendencies, and reci- reacting negatively or refusing to continue. procity/sense of fairness. Specifically prosocial behavior has been studied, Preston and de Waal suggest a model for concentrating either on the choices producing inequity empathy divided into ultimate and proximate or on responses to inequity. Typically individual A levels.148 De Waal149 suggests that state matching and makes choices that can lead either to reward being ‘emotional contagion’ probably evolved with parental received only by itself or also by its partner. Prosocial care, then generalized to other social domains such as choices prevail in both monkeys and apes studied, courting and predator defense. Higher empathy levels and, particularly for ‘second-order inequity,’ depend evolved, allowing more effective support for other strongly on the value of the relationship. group members, some requiring perspective taking, Certain other conditions seem to be necessary for an ability more prevalent in large brained species inequity aversion. Interactions should be continuing, such as apes, elephants and dolphins. However, he not one-off. Partners should see each other. A task does consider that empathy is characteristic of all must be involved; freely given rewards produce mammals and likely birds, or at least some avian no effect. For chimpanzees, disadvantaged inequities species. All these states would require some level of must occur at least 50% of the time; otherwise it sentience. is tolerated. This is reasonable, for in the natural Emotional contagion, has been demonstrated in world, inequities can even out over time and mice (Mus musculus), whose writhing in response to tolerance can promote cooperation. Close social the pain from an injection of acetic acid was exacer- relationships are essential, taking precedence over bated if they observed a cagemate similarly writhing kinship. Indeed the inequity response is more common in pain; general sensitivity to pain, even from a dif- with highly socially cooperative species such as ferent source, was also increased. However social those that hunt in groups and form coalitions

502 © 2013 John Wiley & Sons, Ltd. Volume 4, September/October 2013 WIREs Cognitive Science Cognitive ethology and alliances, irrespective of brain size, or social usually considered to be uniquely human; a strong organization.149,155 Critics emphasize frustration and case is made from caching abilities of some corvids. contrast effects as explanatory mechanisms.156,157 de Natural animal communication studies have revealed Waal and colleagues stress the need for expanding information within some signals that appears to research to more species and to observations of designate specific predator and predator classes and naturally occurring fairness, such as necessary in also descriptors such as size, shape, color, and a chimpanzee alliances and in the play of canids potential predator’s speed and behavior, some of (Canidae) and other species. In play, one who which, however, may simply be correlates of urgency. plays too roughly, or doesn’t ‘apologize’ for it Research has concentrated on vocal alarm calls, can be excluded from future play.158 Although no and should be extended to the more difficult task species exhibits the broad sense of fairness shown of understanding communication not affording such by humans, aspects are present in many species and conspicuous responses to signals. Animals, often, situations.159 but not exclusively, the great apes and corvids, have shown remarkable instances of problem solving and novel tool creation and use, both in the field OTHER ASPECTS OF COGNITIVE and in controlled captive conditions. The study ETHOLOGY of behavioral strategies utilized in anti-predator activities has benefited from taking an intentional Cognitive Ethology is a broad field, encompassing stance, thereby generating hypotheses and detailed too many areas to be dealt with here, including data collection not typically gathered; the Piping meta-cognition, imitation and culture, navigational plover’s use of the broken-wing display is an abilities, animal artificial language and cognition example. A burgeoning field of investigation into projects, Theory of Mind, and deception. Laboratory the evolutionary origins of human senses of justice experimentalists and field scientists can be at odds, and morality has shown widespread instances of with those who have restricted their experience to concern for ‘fairness’ and ‘inequity aversion’ in the the laboratory to tend toward much more minimal species studied, but should be extended beyond interpretations of animal achievements (as in animal primates and dogs. The behavioral expression of culture)160 than would most ethologists.161 such concerns depends on many factors, particularly social bonding strength and likelihood of a continuing relationship; the field is not without controversy. CONCLUSION And controversy still exists over the definitions Over the last decade, there has been enormous of many abilities, particularly as they relate to interest in and research relevant to Cognitive human abilities; examples include consciousness itself, Ethology, the field begun by Donald R. Griffin. episodic memory in animals, tool use, deception, Given the evidence, perhaps particularly that from and morality, among others. However, we should nonintrusive techniques finding similar brain activities attempt to understand those capacities in relation and correlated behaviors in human and other species, to the organism’s particular ecological and social a scientist is hard put to deny at least some level needs, not merely defining them in terms of human of consciousness to nonhuman animals or to claim capacities. that it is not a subject for scientific study. In 2012, Varied research efforts have underscored the prominent neuroscientists signed the Cambridge importance of careful, detailed observations by Declaration on Consciousness asserting that evidence experienced researchers of animals behaving in their could not support humans as the unique harbors of natural environments. From these can arise the consciousness. The questions become which animals hypotheses to be further investigated by additional are conscious, to what levels, and what best ways to observations and field and laboratory experiments. investigate the phenomena. When experiments in the lab contradict plausible It is also clear that exceptional intelligences may interpretations of behavior observed in the wild, exist for different species only in particular modular scientists must be wary. The laboratory is a domains, as driven by ecological and social factors highly circumscribed situation; experimental design impacting on their evolution. Advanced cognitive should allow for possible advanced capabilities abilities have been found in diverse species, including to be demonstrated. We need to be aware of those with vastly different neural organization such possible unrecognized assumptions about an animal’s as the octopus, an organism deserving of further perceptions and goals. We must realize possible study. Some species exhibit episodic-like memory, impacts of boredom, of fear, of the salience of

Volume 4, September/October 2013 © 2013 John Wiley & Sons, Ltd. 503 Advanced Review wires.wiley.com/cogsci the organism’s sensory system. In the end, in the admonitions to be mindful of the Umwelt of the beginning, we must return again to von Uexkull’s¨ animals we wish to understand.

ACKNOWLEDGMENTS I thank Donald R Grifﬁn for his continued inspiration; he would have been pleased to witness the burgeoning interest and advances in ﬁelds in and related to Cognitive Ethology. I also thank W. John Smith, Con Slobodchikoff and Marta B. Manser for helpful discussions and/or manuscripts, as well as the WIREs editors and staff, including Luca Tommasi for useful suggestions and Julie L. Nash for general assistance. I gratefully acknowledge Barnard College and Columbia University for use of library facilities.

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FURTHER READING Hanlon RT, Messenger JB. Cephalopod Behaviour. Cambridge: Cambridge University Press; 1996, 232. Heinrich B. Mind of the Raven, Investigations and Adventures with Wolf-Birds. New York: Cliff Street Books (Harper-Collins); 1999.