Cognitive ethology

Advanced Review

Cognitive ethologyCarolyn A. Ristau∗

Cognitive Ethology, the field initiated by Donald R Griffin, was defined by himas the study of the mental experiences of animals as they behave in their naturalenvironment in the course of their normal lives. It encompasses both the problemsdefined by Chalmers as the ‘hard’ problem of consciousness, phenomenologicalexperience, and the ‘easy’ problems, the phenomena that appear to be explicable(someday) in terms of computational or neural mechanisms. Sources for evidenceof consciousness and other mental experiences that Griffin suggested and areupdated here include (1) possible neural correlates of consciousness, (2) versatilityin meeting novel challenges, and (3) animal communication which he saw as apotential ‘window’ into their mental experiences. Also included is a very briefdiscussion of pertinent philosophical and conceptual issues; cross-species neuralsubstrates underlying selected cognitive abilities; memory capacities especially asrelated to remembering the past and planning for the future; problem solving,tool use and strategic behavioral sequences such as those needed in anti-predatorbehaviors. The capacity for mirror self-recognition is examined as a means toinvestigate higher levels of consciousness. The evolutionary basis for morality isdiscussed. Throughout are noted the admonitions of von Uexkull to the scientist toattempt to understand the Umwelt of each animal. The evolutionary and ecologicalimpacts 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

‘What is it like to be a bat?’. . . the title ofa philosophical essay by Nagel.1 He argued

that we could never know what such an experiencewas like, for as human beings/scientists, we have noway of determining or understanding the nature ofany bat mind state. In correspondence with Nageland in his writings, Donald R. Griffin2,3 the founderof ‘Cognitive Ethology’ argued otherwise. . . that itwas indeed possible to make at least a start intosuch investigations, and even, assuming evolutionarycontinuity of mental experience, to imagine someof the experiences of other organisms. CognitiveEthology was to be a beginning scientific explorationof the mental experiences of animals, particularly as

∗Correspondence to: [email protected]

Department of Psychology, Barnard College of ColumbiaUniversity, New York, NY, USA

Conflict of interest: The author has declared no conflicts of interestfor this article.

they behave in their natural environments in the courseof their normal lives. The mental experiences included,among others, awareness, purposes, consciousness,and general and specific cognitive capacities.

His endeavor provoked considerable contro-versy. But as Griffin had earlier remarked in 1958,concerning biologists’ great reluctance to considerthe possibility of animals’ use of sonar for echolo-cation (now well established), ‘Excessive caution cansometimes lead one as far astray as rash enthusiasm.’4

He proposed exploring several lines of evidencefor this new field: (1) possible neural correlates ofconsciousness; (2) versatility of organisms in adaptingto new challenges for which they have not beeneither genetically prepared or had pertinent learningexperiences; (3) communication by animals, that canbe interpreted as reporting subjective experiences.

Findings have potential impacts on humanbehavior. We are more likely to be concerned aboutanimal’s well being and conservation of their habitatif we understand them to be conscious, intelligentbeings.

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A BRIEF FORAY INTO PHILOSOPHICALISSUES CONCERNING COGNITIVEETHOLOGY

Awareness and ConsciousnessThe problems Griffin raises about consciousness arewhat the philosopher Chalmers,5 in a seminal paper,has termed the (phenomenal) ‘hard’ problems and the‘easy’ problems. The latter, in Chalmers’ view, arethose in which, using methods of cognitive science,the phenomena appear to be explicable (someday) interms of computational or neural mechanisms. The‘easy’ problems entail cognitive abilities includingdiscriminating, integrating information, deliberatelycontrolling behavior, and accessing and reportingmental states among others. (It should be notedthat many scientists would consider that such ‘easy’problems require more than a neural/computationalapproach, a very reductionistic type of explanation.)The ‘hard’ problems are the phenomenological ones,the very experience of a mental state, a perception,a pain, ‘what it is like to be xxx.’ In the past,most scientists have avoided the ‘hard’ problems.Many philosophers, however, including Aristotle,6

Descartes,7 and contemporary philosophers ofmind8–11 have been concerned with issues of animalconsciousness and reason. The philosopher Searle12,13

is probably most closely aligned with the stances ofGriffin, and considers that a main issue is not whethernonhuman animals are conscious, but which animalsare conscious and to what level of consciousness.

Even Darwin entitled a book ‘The Expression ofthe Emotions in Man and Animals.’14 As Griffin notes,Darwin’s inclusion of mental continuity in evolutionis far more reasonable a scientific approach thanbeginning with the denial of such capacity. Griffinfurther suggests that a yet more conservative, neutralapproach would be to assume p = 0.5 with respect tothe probability of consciousness in animals and thento increase or decrease that probability as data areaccumulated.15

Nevertheless, despite confusion over definitions,more (not all) contemporary animal behavior sci-entists appear to grant, to at least some species,phenomenological ‘awareness’ or ‘primary conscious-ness,’ if not the higher levels of consciousness. Thosehigher levels are often termed ‘sentience,’ describedas the depth of awareness of self and others. Sen-tience includes self-awareness (both self as a bodyentailing self-recognition and self including a men-tal entity existing in a continual fashion in thepast, present, and future), metacognition (the abil-ity to think about the contents of one’s own mentalstates/feelings), and Theory of Mind (various abilities

including perspective taking, empathy, and generallythe ability to model another’s mental and physicalperspective).16–18

Approaches to the Study of AnimalCapacitiesA significant contribution to the study of animals is theconcept von Uexkull19 proposed in 1909, that of the‘Umwelt,’ meaning the environment as an organismperceives it and interacts with it. Several organismscan appear to live in the ‘same’ environment, butin effect those environments are vastly different,with each organism sensing and emphasizing differentaspects, interacting differently, using the environmentdifferently.

Another approach to species comparisons isa ‘functional’ one. Thus ethologists describe andcompare foraging strategies, food preparation/storage,territory selection/defence, selection/creation of ahome, mate selection, parenting behavior and theconcomitant cognitive skills required in each. Wehave learned that cognitive abilities in one sphereneed not generalize to another. Such modularity raisesthe issue of ‘what’ has evolved?What circuitry? Arethere ‘core knowledge systems’ common to humansand some other species20–22 or can abilities in onesphere generalize to another(s). . . over the eons orpossibly in an organism over a lifetime? We do findmany examples of one available biological ‘solution’being used over evolution for other purposes.23

Truly appropriate comparisons of abilitiesacross species likewise entails understanding thedevelopmental and learning processes involved: doesthe capacity occur full-blown in all species members?What experiences/learning trials were required; howmany; over how long a time?

Work with captive species has revealed abilitiespossibly latent in the natural environment. In a fewinstances, captive great apes have been observed toactively teach as distinguished from exhibiting abehavior which may be copied. For example, thesigning chimpanzee (Pan troglodytes) Washoe activelymolded the hands of young chimpanzee Loulis intothe sign for food, a training technique often usedby humans with Washoe.24 Some captive apes, inparticular, young apes, achieve abilities not observedin the field, e.g. spontaneous pointing, and do so morereadily if they have more (positive) interactions withhumans.25 Even monkeys can be specifically taughtto point and then they generalize to use the skill in acommunicative manner in varied circumstances.17

We need to recognize that some observedbehaviors may be ‘default,’ those exhibited in urgent

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WIREs Cognitive Science Cognitive ethology

circumstances or in the presence of very potent stimuli,and can be detrimental in that particular situation. Inless constrained circumstances, the organism may havereacted differently. For example, the beavers’ cognitiveabilities utilized in dam construction and repairhave been denigrated, because some experimentalwork indicated that a beaver plastered mud overa loudspeaker that produced white noise, a soundsimilar to water rushing through a leak.26 Thatbehavior can likewise be interpreted as a usefulfailsafe, while dam repair is achieved more flexiblyin many circumstances.27

In short there is a need for cautious conclusionsand openness to various approaches.

NEUROLOGICAL ANDNEUROANATOMICAL ISSUES

Neural Correlates of ConsciousnessDespite intensive efforts to date (2012), research tofind Neural Correlates of Consciousness (NCC) hasnot revealed structures or processes unique to humansthat are necessary for consciousness. It must also benoted that neither have any necessary and sufficientneural correlates of consciousness been determined.We have learned that consciousness involves manylevels of brain functioning from brainstem to thecortex.28

A proper discussion of NCC is beyond the scopeof this ms. Refer to Griffin and Speck17 or resourcesconcerning neural studies and theories as they relateto the possibility of demonstrating consciousness innonhuman animals.29,30 Evidence includes pharmaco-logical interventions that can affect human consciousbehavior, use of human consciousness studies, such asbinocular rivalry and blindsight and relating all theseto similar investigations and behaviors in nonhumans.Further supportive evidence for widespread conscious-ness is offered by Panksepp’s research31 emphasizingdeep, old subcortical systems that generate affectiveconsciousness and emotional expression. Quite sim-ilar systems occur in all mammals and some birds.When stimulated in humans, they produce intenseemotional feelings and associated behaviors. In non-humans, stimulation produces similar behavioral andphysiological responses and, it is interpreted, similarconscious feelings. Not all agree.

Referring to this and other research, a groupof eminent cognitive scientists recently signed the‘Cambridge Declaration on Consciousness,’ basicallystating that humans are not unique in possessing theneurological substrates that generate consciousness.32

Brain Structures Underlying CognitiveCapacitiesDespite current disagreements about directly linkingspecific neural activity or areas with consciousness,certain brain structures have been shown to play sig-nificant roles in both humans and other species, under-lying similar kinds of cognitive competencies. In par-ticular, the hippocampus (in vertebrates) is intrinsic tolearning and storing spatial information, such as land-marks, distances and directions, all of which can figureimportantly in locating food, territory and dwellingsites, scatter hoarding, migration, and mating.33

Some avian species, particularly corvids, typ-ically investigated in the laboratory, exhibit aston-ishing abilities to cache food for times of scarcity,some species retrieving in a matter of hours, othersin months.34 Hippocampal size varies with spatialdemands placed on animals by their ecology, withincreasing neurogenesis rates for winter storage anddeclines during spring. For example, in black-cappedchickadees (Poecile gambeli) large differences in mem-ory and hippocampal size occur over both largecontinental scale differences in winter severity as wellas over small spatial scales that occur with the increas-ingly harsh conditions as one ascends a mountain;significant differences occur over as little as 600 mof elevation.35,36 Hippocampal size also varies withmating systems; polygamous species needing to roamover larger territories to find mates have a largerhippocampus than do monogamous species.37

Homologous brain structures have been soughtfor the language learning of human children and non-human animals’ vocal communicative development.Many parallels have been found in avian song learn-ing such as babbling and sound crystallization. Yet,among primates, it is chimpanzee gestural communi-cation that may provide interesting parallels as wellas possible homologous neurological structures.29,38

Relative brain size with respect to body weightshows parrots and corvids (such as crows, rooks, andjays) are comparable to chimpanzees, with humanstopping the list; dolphins particularly, but even seals,also have high ratios. Generally that greater relativebrain size is associated with advanced cognitiveprocessing and with high levels of sociality, longevity,slow development and long parental investment aswell as a large forebrain.39 Interestingly it is differentbrain structures that show these correlations. Inhumans and other mammals, it is the cortex; in birdsit is the nidopallium, until recently not considered ahomologous structure.37,40

Forebrain size has been linked to differentabilities in different species. In birds, the linkageappears to be to innovative behavior. In ungulates



and primates forebrain size is linked more closely tosocial dynamics41 such as intra-group co-ordinationand aspects of group size; linkage may also be to thetype and quality of bonding relationships.42

In fact the most pertinent commonalitiesbetween primates, including humans, and birds, arevirtually identical neuronal connections and microcir-cuits that have been recently identified as mediatingsimilar behaviors.43

Very different neural systems can subservecomplex behaviors, namely that of cephalopods,particularly the octopus, likely squid, possiblycuttlefish.44–46 The octopus nervous system has threemain parts: a large brain of two central masses, thearm nervous system, and optic lobes. The systemconsists of about 500 million neurons, in contrastto rats’ 100 million and dogs’ 600 million.47 Thatbrain is among the largest of any invertebrate and thebrain/body ratio of Octopus vulgaris is comparable tothat of lower vertebrates.48 The octopus may haveundergone convergent evolution with vertebrates,needing extensive memory and learning perhapsdriven in part by its being a solitary hunter orexacerbated by its vulnerability due to loss of theancestral shell.49 The mammalian hippocampus andoctopus MSF-VL system in the large brain lobesare similar, specifically in architecture, physiologicalconnectivity and the exceptionally high number ofsmall interneurons in the learning and memory areas.Convergence is not complete, with typical invertebrateneural communication, particularly with respect tocell structure and membrane properties. However,like those in other species, activity-dependent synapticplasticity exists in neural areas important for learningand memory.50

In conclusion, the hippocampus and otherbrain structures are subserving similar and complexfunctions in different species. The critical aspectappears to be similar micro patterns of individualneural connections rather than the brain region per se.

SENSING (AND INTERACTING WITH)THE ENVIRONMENT

As emphasized in von Uexkull’s concept of Umwelt,nonhuman animals’ sensory systems differ from eachother and from humans, not only in sensing capacities,but also in senses emphasized and means of gatheringand utilizing the sensory information. A chimpanzeein a signing project initially learns not that thesign for flower signifies ‘flower,’ but rather the ape,presented with a flower, generalizes to associate thesign with other odors such as pipe tobacco andkitchen fumes.51,52 An elephant appears incapable

of the Mirror Self Recognition test until the paradigmincludes the opportunity to explore a larger mirrorwith the tip of its trunk.53

The capacities can be different as in the honeybee’s detecting both polarized light, and, like manyother insects, UV light. To some, UV signifies openspace, not the dark nest, for the sun is the onlynatural source of UV. To the honeybee, UV light alsoallows perceiving floral patterns that provide ‘paths’to nectar/pollen. In von Uexkull’s famous example,a tick sucks not a human, but the rock wet withbutyric acid from the sweaty man no longer there.The horse’s visual system allows it to detect somethingvery well along the horizon, but in other regions, ithas somewhat reduced acuity; this is attributed to along streak of ganglion cells across the retina whichparallel the slit-like pupil of the horse’s eye.54

What is to be constructed from the sensorysystems is another matter. ‘Search image’ has beenproposed as a learned and/or innate sensory patternfacilitating an organism’s finding a particular foodtype, especially cryptic ones. On the other hand,simply detecting change in the environment and/orfrom a learned sensory pattern is critically importantfor ‘lower’ species such as sharks and lobsters; acutesensitivity to changing odor concentration in watercurrents can lead the animals to the source, food.55

Cross-modal matching is achievable by horses (andother species); horses can discriminate by voice cuesbetween a familiar and unfamiliar person, then matchvoice to visual/olfactory cues.56

We likely have not yet discovered the full array ofother organisms’ sensory capacities; adaptive behaviorof some species before earthquakes or approachingstorms suggests sensitivities we do not know.

ANIMAL COMMUNICATION

Natural Animal CommunicationAnimal communication encompasses a broad array ofsignals, including visual, acoustic, electromagnetic,vibration, and odor. The focus here will be onvocal communication, which has received extensiveinvestigation, probably because auditory signalscan readily be recorded, then used in ‘playback’experiments.

Among the core issues are: (1) whether signalsare emitted in a reflexive, emotive Groan of Painmanner as Griffin termed it,57 or via an InnateReleasing Mechanism (IRM) as earlier described byTinbergen58 or whether some voluntary control exists.(2) the meaning of the communication. Indeed Griffinsaw animal communication as ‘a window on animalminds.’2 (3) then, how to investigate these issues?



Voluntary Usage?The issue was addressed with the concept ‘audienceeffect,’ which examines the impact of a particularconspecific’s presence on the likelihood of acommunicator uttering a given vocalization.59,60 Forexample, a male might make ‘food calls’ in thepresence of food and a female, but not if anothermale were present instead of the female.

In analyzing animal vocal communication, sci-entists differentiate between (1) the acoustic structureof the call, (2) the usage, and (3) comprehension,distinguishing between information that a scientistrecognizes in the call and the recipient(s)’ comprehen-sion and utilization of that information.

Many factors may impact on whether a potentialvocalizer calls and whether the recipient actuallyresponds and how. These factors, addressed alreadyin 1977 by Smith,61,62 include past history of theorganism, likely unknown to the researcher. Suchconcerns are not limited to ‘intelligent’ organisms;familiarity and social history have been shown toaffect the signaling of Siamese fighting fish.63

Meaning of SignalsSmith64 encouraged a ‘message-meaning analysis’ ofsignals, noting that the same auditory productioncan have different meanings, depending on recipientand context (including past history, environment,and other stored information). Thus a male bird’sspringtime song may mean to another male ‘likelyaggression by me if you approach’ or ‘come hither’to a female. Messages may include informationabout the signaler’s behavior and probability thereof,location, individual or group identity, or externalreferents such as predators, food, events or other‘things.’ Message-meaning analysis requires detailedobservations about correlations with conditions andsignaler and recipient(s)’ behavior, prior to, duringand after the signal. It is difficult to do well.

A simpler methodology, with significant lim-itations, but widely adopted probably due to thatsimplicity, relies on ‘functional referents.’ Calls are soclassified if they appear to be highly stimulus specific65

and if call recipients use that specificity to determinethe nature of their adaptive response.66–70 This anal-ysis sidesteps the issue of information contained inthe call, requiring a ++ behavioral response as evi-dence for the ‘functional referent;’ it has thus beenused primarily with so-called ‘food ‘ and ‘alarm’ calls.Concerns with this analysis and the playback experi-ments typically used, center on the lack of contextualinformation available to a recipient with which tocalibrate responses, and thus a higher likelihood of a‘default’ or fail-safe response.63,71

Presently, scientists are attempting to fine tunetheir approach to studying signaling, including morestudies beyond alarm and food calls. Smith’s suggestedanalysis, though difficult, can help elucidate signalinformation. Townsend and Manser,70 in their excel-lent review, suggest variants of playback experiments,including prime-probe, habituation-dishabituationand violation of expectation techniques.

Information in Alarm CallsMost scientists agree that alarm calls containurgency-based information (predator’s threat level).Interpretation of the referential component of callsis much more controversial. Apparent categoriesof functionally referential information potentiallyavailable in an alarm signal are: predator type (aerialor terrestrial, specific species), predator’s spatiallocation, physical qualities such as size, shape, andcolor, and predator behaviors such as movement (nomovement, speed, kind of movement such as hawkperched, searching for prey or attacking72).

Initial distinctions between calls for aerial andsome ground predators were noted from astute obser-vations of vervet monkeys (Cercopithecus aethiops)by an experienced field researcher (Struhsaker)73 andwere then followed up by videotaped playback experi-ments in the field.64 Since then, acoustically distinctivecalls for aerial and for ground predators have beenfound in a diverse number of species, including chick-ens(Gallus gallus domesticus),66,74 many species ofground squirrels (Spermophilus spp.),75 tree squir-rels (Tamiasciurus hudsonicus),76 social mongooses(aka Meerkats) (Suricata suricatta),77 prairie dogs(Gunnison’s (Cynomys gunnisoni) and Black-tailed(Cynomys ludovicianus)),78 and various lemurs79 andmonkeys80–83 (reviewed in Ref 84). For some speciesthe calls appear to be quite specific in their refer-ents, for example, the vervet monkeys have threetypes of calls causing differential responding, forexample, looking upward and running to a nearbybush to the call for eagle-type predators, lookingto the ground for snake-type calls and running upinto the trees or remaining quietly there for calls forleopard-like predators.64,72 [These responses, how-ever, are not absolutely unique to each predator type,with occasional similar responses across categories asindicated in both the original and more recent data.Recent studies also show a sex difference, with onlyfemale vervets exhibiting the distinctive responding(J. Fischer, personal communication)]. Social mon-gooses calls distinguish aerial versus ground preda-tors at different urgency levels.85 Various species ofprairie dogs appear to have both distinctive calls andappropriate responding behavior to the calls for at



least four different potential predators (coyote (Canislatrans), domestic dog (Canis familiaris), red-tailedhawk (Buteo jamaicensis), and human (Homo sapi-ens)75,86,87) and also possibly to badgers (Taxideataxus),88 ferrets (black-footed (Mustela nigripes)89

and snakes, including specific snake species.90 Some-times species have both specific and broadly usedalarm77 and mobbing calls.91 There is evidence aswell for some interspecies recognition of alarm calls(discussion in Ref 92).

Some of the most perplexing interpretations ofdata are for alarm calls said to denote predatorcharacteristics such as size, color, or shape. Thesedistinctions have been reported for prairie dogs,85,93

but black-capped chickadees also appear to encodeinformation about predator size,94 and male chickensprovide graded information about aerial stimuli size,distance and speed, to which captive females respondin graded fashion in experimental situations.95

Is some call information (e.g., size, speed, dis-tance) merely a correlate of urgency? Slobdochikoff’sexperiments argue against that interpretation, in thatacoustic structure of prairie dog alarm calls variedwith colors on intruders and were distinctive for cer-tain geometric shapes (triangle vs. circle–square).96

Slobodchifkoff (pers. comm.) suggests that the geo-metric sensitivities may be related to the prairie dogs’predator classes: triangular for raptors, circular–rect-angular for mammalian ground predators.

PlasticityPlasticity, originally thought to be the property onlyof human language, has been found in song birds(Oscines), then in hummingbirds (Trochilidae) andparrots (Psittaciformes)97 and then more widespread.Some species show gradual development to the adults’more complex acoustic alarm calls (e.g., prairie dogs,meerkats).Prairie dogs have been shown to modifycalls made to a human intruder if that intruder becamemore threatening (e.g., fired a gun). Goat (Caprahircus) contact calls have been shown to exhibit plas-ticity, affected both by kinship and membership indifferent social groups.98 These differences potentiallypromote mother-kid recognition, individual identity,and the formation of ‘dialects’ indicative of socialgroup membership. Growing evidence supports vocalproduction learning in some other mammalian species:bats, pinnipeds, cetaceans and elephants (discussion inRef 97). There are scattered references to refinementof usage93 and development of unique food calls insome primate species.99

Further QuestionsHow to conceptualize present findings in animalcommunication? Analysis has been greatly facilitated

by the introduction of discriminant functional analysis(DFA) and other statistics,100 replacing some ofthe tedious measurement and possible subjectivityin classification. Acoustic structural differences doreliably sort calls according to descriptors such ascolor, size, and shape and other conditions, but, inmany cases, we are unable to provide evidence, at thispoint, that call recipients are using that information.

Why do such complex communication systemsexist in some species? The alarm systems ofprairie dogs and meerkats may have resulted fromevolutionary pressures deriving from their ecologicalconditions. For example, prairie dogs are a fixed socialspecies, subject to the same predator individuals,with fairly set escape opportunities (bolt holes andtunnels).101 Some individual predators have differentstrategies: some coyotes rapidly charge at any prairiedogs; others wait at a well-populated burrow.102 Itwould be beneficial to recognize those individuals,perhaps aided by color or shape information. Thefield needs further explorations of communicationcomplexity across species and ecological conditions.

Caching, Episodic Memory, and MentalTime TravelWhether animals have episodic memory remainsdebated still, Tulving103,104 having claimed it to be auniquely human capacity. Episodic memory (‘remem-ber’) is distinguished from semantic memory (‘know’).To remember, for Tulving, includes recognizing thatit is oneself in the past episode and in the present; thatassertion is most difficult to establish in a nonlinguis-tic organism. Evidence supports close relationshipsbetween episodic memory and the ability to projectoneself into the future, with shared neural systemsand developmental paths.105,106 Planning for oth-ers seems to precede developmentally planning forself, a distinction Clayton suggests may be useful inanimal studies.104 Whatever the difficulties of interpre-tation, there have been useful criteria established forinvestigating ‘episodic-like’ memory in nonhuman ani-mals: (1) the what–where–when paradigm, and (2) the‘unexpected question’ technique.

In a set of ingenious experiments, Claytonand colleagues, allowed scrub jays (Aphelocomacoerulescens) to bury larvae, a preferred food and,in a separate place, peanuts, less preferred.107 Thebirds had learned that the larvae decay and becomeinedible after five days, but the peanuts do not. Given achoice soon, or after five days, the scrub jays chose theappropriate spot to retrieve the food. This experimentfulfilled the what-where-when conditions. However,subsequent research indicated limited success beyond



the food caching corvids, and only scrub jays met allthe conditions the researchers set.

The ‘unexpected question’ paradigm suggestedby Zentall108 tests for something that was incidentalat the time of training (presumably ‘unattended’ bythe animal), using a probe trial inserted within theordinary testing trials. As Clayton et al note, a usefulapproach for future studies.

PROBLEM SOLVING, TOOL USE, ANDSTRATEGIC BEHAVIOR SEQUENCES

Problem SolvingKohler109 set chimpanzees problems to acquire out-of-reach food, having boxes available that could bepiled up or poles that could be fit together. Kohlerreported that the chimpanzees solved these problemsspontaneously, not by stimulus–response associationor trial and error, but by a sudden insight. There areother interpretations of the chimpanzees’ behavior.Many other species were subsequently also seen to becapable of various problem solving tasks.

Some of the most remarkable understandings,interpreted as comprehending causal relations, areexhibited in Heinrich’s experiments with ravens(Corvus corax).110 In one set, adult captive ravenswith no experience with strings, after several hours,pulled up meat dangling on a meter long piece ofstring. They pulled up sections, stood on the capturedstring, and repeated this motion until reaching themeat. If startled, ordinary ravens fly off with any foodin their mouth. In this experiment, a raven who wasunsuccessful at pulling up the food, did try to fly awaywith meat on a string, but those who had pulled up themeat did not do so, even on the first startle. In otherexperiments with crossed colored strings, one holdinga rock and the other meat, some ravens immediatelypulled on the correct string. Other ravens did so aftera brief tug moved the unpalatable rock. However theypersisted over subsequent trials in initially pulling theincorrect string, directly under which hung the rock,then corrected and pulled the string which moved themeat. Another task, with different ravens and a loopedstring which ‘illogically’ required pulling down on thestring to move the meat up was never successfullysolved and the ravens lost interest. We do not knowall causal relations or ‘physics’ the ravens understand,or the ‘rules’ they apply, but gradually, across species,we may be able to determine ecologically appropriategeneralities.

Tool UseIn the wild, tool use has been observed in a wide arrayof taxa, including all great apes, some monkeys, some

birds, particularly the corvids, some cetaceans, fishes,invertebrates including octopi, and, surprisingly, inonly five species of nonprimate mammals. Veinedoctopi (Amphioctopus marginatus) have been filmedcarrying discarded coconut shells along as they walk,requiring an ungainly inefficient ‘stilt walk’ to doso, then using the shells for protective shelter asneeded.111

The mammals observed using tools in thewild are some Asian elephants (Elphas maximus)which modify branches to swat away flies, sea otters(Enhydra lutris) which frequently use rocks to breakthe shells of clams and sea urchins, some bottle nosedolphins (Tursiops sp) using sponges to protect bodyparts while foraging, humpback whales (Megapteranovaeangliae) which blow bubble curtains used totrap fish schools , and as recently observed, brownbears (Ursus arctos) which scratch themselves withselected, barnacle encrusted rocks.112 The topic hasseveral extensive reviews113–116 and will be mentionedonly briefly here.

In captivity, various species, not observedusing tools in the wild, have been taught tooluse, including rooks (Corvus frugilegus)117 andwood pecker finches (Cactospiza pallida)118 or haveindependently demonstrated tool creation and use.18

One of the more remarkable instances of tool creationinvolved captive New Caledonian crows (Corvusmoneduloides). A female crow, having seen a wirehook, but never having witnessed the process ofbending wire, nevertheless, bent a wire into a hookto reach food down a tube. This creation involvedinnovative behavior and nonnatural materials, notlikely to be encountered in the wild.119

The definition of tool use is a continuingdebate, but most scientists agree that it requiresthe manipulation of a freely movable object on atarget object to modify the target object’s physicalcharacteristics.113 Using tools is of especial interestbecause it implies a goal or purpose, requires atleast short-term planning (sometimes longer) and,depending on the context, can require flexiblebehavior. Some species can also modify their toolsto be more efficient.

The definition of tool use can also beextended.111 For example, Tinbergen reportedHerring gulls picking up clams (movable) andopening them to eat by dropping them onto rocks(stationary).120 A gorilla used a stick apparently todetermine water depth, thus improving its access toinformation.121 Mike, the well known Goodall studychimpanzee, improved his display by loudly bangingdiscarded kerosene cans, such continued usage finallyresulting in a rise in his status.122



Given the diversity of species capable of tooluse and the various specialized uses, it is likely thatthere are different cognitive mechanisms and differentecological and social constraints/drivers underlyingthe capacity, as is true of many cognitive abilities.

Strategic Behavior SequencesIntroductionStrategic behaviors exhibited by animals can revealboth cognitive complexity and intended behavior.The behaviors are relevant to issues of representationand intentionality, both in the philosophical senseof intentionality and ‘intended’ or ‘purposeful’(included within a concept of intentionality).123

Several aspects of strategic behaviors are of particularinterest to Cognitive Ethologists: organisms mustbe able to prioritize between conflicting demands,for example, courting, mating, feeding self, feedingyoung, protecting young, hunting, avoiding predation.Animals also often need to use spatial information,recognize and take advantage of opportunistic events,overcome obstacles, especially novel ones, learnthrough either actual or mental trial and error, andsometimes even deceive.

Great apes’ strategic behaviors are welldocumented,124,125 so I will note lesser known cases,firstly, those of an ungulate, the pronghorn antelope(Antilocapra Americana).126 Their complex antipreda-tor behavior also supports evolution of a specializedintelligence, not via the social intelligence hypoth-esis,127 but rather from the driving force of predation,in the antelopes’ case, particularly on the young.

Predator Avoidance Behavior/Protecting Young:AntelopesIn general, ungulate adults avoid predation bybeing large bodied and/or fast runners. However,as reported by Byers,118 mother pronghorn antelopehide vulnerable newborns, staying away and, beforereturning, run about, even for a half an hour, oftenstaring, appearing to look for predators. The highpredation pressure at Byers’ site, results in 75–100%of the fawns falling to coyotes or eagles.128,129 Byersreports a returning mother suddenly seeing two low-flying golden eagles. The doe leaves the young’sregion, craning back her head, a posture used onlywhen looking at golden eagles. She then waits 30 min,departing again when the eagles return.

With coyotes, Byers reports that the antelopemother, usually positioned far from the young (about70 m), extrapolates from the coyote’s path, distractingonly when the coyote’s path will intercept the fawns.She then flashes her large white rump patch andprances distinctively.

Protecting the Young: Injury Feigning BirdsSome ground nesting birds when having a nest oryoung, will perform various apparently distractivebehaviors in the presence of a predator or intruder.For the Piping plover (Charadrius melodus), theseinclude flying conspicuously in front of the intruder,vocalizing near the intruder, ‘false brooding’ (sittingfluffed out on a site where there is no nest), orthe most dramatic, engaging in very awkward wing-flapping, commonly termed ‘broken-wing displays’or ‘injury feigning.’ So ‘injured,’ the bird maydisplay, sometimes for many minutes or for hundredsof feet, but then simply flies away. The birdsgive an impression of trying to lead the intruderaway from the nest, though some have claimedthe movements are ‘hysterical’ and others haveclaimed the movements are released and directedthroughout by sign stimuli.130 Ristau131 investigatedthe possibility that the behavior is purposeful,applying what Dennett has termed a first orderintentional stance,8 namely that ‘the plover wantsto lead the intruder away from the nest/young.’A purposeful interpretation suggests the followingpredictions: (1) the plover should move in a directionsuch that an intruder following it would movefurther from the nest or young, (2) the plover shouldmonitor the intruder’s behavior, and (3) the plovershould respond appropriately to changes in theintruder’s behavior.

Ristau found that in 44/45 cases the Pipingplover displayed while moving in a direction thatwould lead the intruder away from the nest. The birddid monitor the intruder and changed its behavior ifan intruder stopped following the display, includingsuch actions as flying or walking closer to the intruderor displaying more intensely.

The bird also chose its location for display,sometimes flying, which, in all cases examined,resulted in the bird being closer to the intruder.The plovers also quickly learned to discriminatebetween humans who had behaved in ‘threatening’ways and those who had not, namely those whopreviously had hovered over the nest and thosewho had simply walked by, not looking at thenest. Only one or two exposures were necessary.Others have interpreted the ‘broken-wing’ behaviorof plover species in a much more minimal way.Byers,123 for example, contrasts the ungulates’‘calculated’ behavior with that of another ploverspecies, the killdeer (Charadrius vociferous). Heclaims the killdeer parents display no matter whathis path, dependent only on his approach distance.However, as demonstrated in the above researchby Ristau129 with a related species, the plover’s



display is not static, but on a path leading awayfrom the young. Readiness to display does appearto depend on previous exposure to humans, birdsinitially being very wary, likely to display anddoing so at greater approach distances. Ristau’sdetailed sequential analysis, adopting the stance ofpossible purposeful behavior, does lead to a deeperappreciation of the complexity of the interactivebehavior, than does simply noting approach distance.This use of the intentional stance is instrumentalin nature, helpful in suggesting experimental workand meaningful kinds of observations. As variousphilosophers and scientists have suggested, furtherconceptual work is needed to better theoreticallyground these and other behaviors studied/analyzedby cognitive ethologists.132

Predatory StrategiesStrategies are also required by the predators. Verywell documented accounts show individual membersof genus X overcome obstacles to reach their prey,taking long detours around, often losing visual contactwith that prey. In danger themselves of predationby their prey, they are opportunistic, moving closerwhen such movements are disguised or the prey isdistracted by other events. Some of the predator’scommunication is highly similar to that used in theprey’s courtship and suffices to mislead the prey.Genus X is any of several jumping spiders, Portia.These large venomous spiders build their own websto capture insects, but also specialize in preying uponother spiders by invading their webs. Portia plucksthe strings of the prey’s web, sometimes similarlyto the prey’s courtship vibrations. Signals that bringthe prey closer to the web edge are continued,otherwise varied. Some signals are like those ofa ruffling breeze or falling leaf. Should a breezeblow, Portia advances, under protection of thosevibrations. Should the prey advance aggressively,Portia retreats. Portia may return, even a half anhour later, but often with a different tactic, perhapsdropping precisely from above, on a silken thread,onto the prey, killing it with a poisonous bite. Inlaboratory experiments, Portia can, on first encounter,successfully capture novel spiders, never encounteredin its evolutionary history.16,133,134 Critics will inventa myriad of complex modules to deal with thesephenomena; others may suspect that some cognitivecapacities may reside in such organisms.

Other Aspects of Predator and Prey BehaviorAlerting predators to one’s presence is a tactic thatis used by many species, when predation appearsto rely on surprise, for example, antelopes produce

a high bounding gait (‘stotting’)135; hares standbipedally.136 And prey likewise carefully monitorpredator activities, seeming able to detect whenpredators are not dangerous, either resting at adistance or otherwise engaged.137

Some predators are capable of co-operativehunting, from simple to complex, particularly in chim-panzees and lionesses (Panthera leo), but observationsexist also of pelicans (Pelacanus crispus), cormorants(e.g., Phalacrocorax auritus), Harris’s hawks (Parabu-teo unicinctus), and likely other birds of prey, SouthAmerican otters (Pteronura braziliensus), dusky dol-phins (Lagenorhynchus obscurus), killer whales (Orci-nus orca), hyenas (notably Crocuta crocuta), and otherspecies.138

MIRROR SELF RECOGNITIONEXPERIMENTS

The mirror self-recognition (MSR) experiments139 areof interest for several reasons. In these, a mark isplaced on an organism where it cannot be seenexcept by the organism’s viewing its own reflectionin a mirror. The successful subject tries to exploreor remove the mark. Human children pass this testbetween 18 and 24 months of age, other species whichsucceed, at later ages. Gallup and later de Waalhave suggested that MSR capacity has coevolved withempathy and perspective taking.140,141 And specieswith those capacities have evolved with complex socialgroup structures and/or interactions.

Although a myriad of species have been tested,from chickens and beyond, only humans, great apes,dolphins (Tursiops truncates),142 Asian elephants(Elephas maximus),51 and magpies (Pica pica),143

the only nonmammalian species, have succeeded.Arguments can be made for homologous evolution inhumans and great apes, but would require convergentevolutionary mechanisms for the other species.

To succeed does not imply having the samecapacity for self recognition that humans do; thatcapacity develops gradually beyond MSR. MSRentails recognition of self as a body, not self as amind, or psychological entity existing in the past,present, and future.

When individuals pass the test, they go throughseveral stages. Initially they (1) give ‘social displays,’reacting to the image as an ‘other,’ often threatening,sometimes courting, then (2) physically inspect themirror, even looking behind it, (3) test for behavioralcontingencies, often passing repeatedly in front ofthe mirror, and (4) inspect the marking. In testswith successful species, not all individuals pass, somestopping at earlier stages or losing interest altogether,



not uncommon behavior for non-MSR tasks too.For gorillas and orangutans, some researchers reportsuccess and others failure.

Why the magpie succeeds at MSR, while parrots,a social and very cognitively advanced species, havenot, is unclear. The magpie is a corvid, stores food,requiring detailed memory capacity, and rememberswho has observed its storing, suggesting strong socialsensitivities.144 Of five magpies tested, clear MSRevidence occurred in two birds, weaker in anotherand not in two.

Why do tests fail for some experiments and somespecies? The successful Asian elephant tests allowedthe elephant to explore the mirror with its trunk, aprimary appendage for assessing its environment,52

and provided a far larger mirror for the elephantto view than had earlier work.145 Interestingly, theelephant used the smaller mirror to locate hiddenfood; such instrumental mirror use without passingMSR has occurred in various species. The directgaze entailed in MSR is, in many species, particularlyprimates, an aggressive communication and so mayimpact on exploration of the image. Despite somedebate about MSR,146 it does appear to requireadvanced cognitive/social abilities and so remains auseful comparative technique.147

MORALITY

Morality is considered by many to have its rootsin emotional and empathetic behavior. DeWaaland colleagues specifically propose roots in empa-thy/consolation, pro-social tendencies, and reci-procity/sense of fairness.

Preston and de Waal suggest a model forempathy divided into ultimate and proximatelevels.148 De Waal149 suggests that state matching and‘emotional contagion’ probably evolved with parentalcare, then generalized to other social domains such ascourting and predator defense. Higher empathy levelsevolved, allowing more effective support for othergroup members, some requiring perspective taking,an ability more prevalent in large brained speciessuch as apes, elephants and dolphins. However, hedoes consider that empathy is characteristic of allmammals and likely birds, or at least some avianspecies. All these states would require some level ofsentience.

Emotional contagion, has been demonstrated inmice (Mus musculus), whose writhing in response tothe pain from an injection of acetic acid was exacer-bated if they observed a cagemate similarly writhingin pain; general sensitivity to pain, even from a dif-ferent source, was also increased. However social

relationships mattered; this occurred only for cage-mate pairs. In fact, males, but not females, showed acounter-empathetic reaction, reducing their own painsensitivity when witnessing the pain of unfamiliarmales, presumably likely rivals.150

A sense of fairness has been investigated,specifically ‘inequity aversion,’ a term from economicstheory. In seminal research with capuchin monkeys(Cebus apella), the monkeys refused to accept apiece of cucumber, a less preferred food that theyhad been exchanging with the experimenter fortokens, when their partner suddenly started receivinghighly preferred grapes instead of cucumber.151

The results set off a flurry of controversy andresearch, discussed in an excellent review byBrosnan and DeWaal.152 Most research entailednon-human primates, and sometimes dogs (Canislupus familiaris), generally indicating negativeresponses to continuing inequity between an animaland a social partner, with the disadvantagedoften refusing to continue the task. Cleaner fish(Labroides dimidiatus) which work cooperatively,punish those not contributing to the cleaning.153

However, in experiments, they did not exhibitinequity aversion, suggesting that punishment,rather than sensitivity to equity, can maintaincooperation.154

What of the other side of injustice, the‘advantaged inequity’ of the one receiving more.This ‘second order inequity,’ considered as derivingfrom the first, and weaker, does, at least sometimeswith chimpanzees, lead to the advantaged individualreacting negatively or refusing to continue.

Specifically prosocial behavior has been studied,concentrating either on the choices producing inequityor on responses to inequity. Typically individual Amakes choices that can lead either to reward beingreceived only by itself or also by its partner. Prosocialchoices prevail in both monkeys and apes studied,and, particularly for ‘second-order inequity,’ dependstrongly on the value of the relationship.

Certain other conditions seem to be necessary forinequity aversion. Interactions should be continuing,not one-off. Partners should see each other. A taskmust be involved; freely given rewards produceno effect. For chimpanzees, disadvantaged inequitiesmust occur at least 50% of the time; otherwise itis tolerated. This is reasonable, for in the naturalworld, inequities can even out over time andtolerance can promote cooperation. Close socialrelationships are essential, taking precedence overkinship. Indeed the inequity response is more commonwith highly socially cooperative species such asthose that hunt in groups and form coalitions



and alliances, irrespective of brain size, or socialorganization.149,155 Critics emphasize frustration andcontrast effects as explanatory mechanisms.156,157 deWaal and colleagues stress the need for expandingresearch to more species and to observations ofnaturally occurring fairness, such as necessary inchimpanzee alliances and in the play of canids(Canidae) and other species. In play, one whoplays too roughly, or doesn’t ‘apologize’ for itcan be excluded from future play.158 Although nospecies exhibits the broad sense of fairness shownby humans, aspects are present in many species andsituations.159

OTHER ASPECTS OF COGNITIVEETHOLOGY

Cognitive Ethology is a broad field, encompassingtoo many areas to be dealt with here, includingmeta-cognition, imitation and culture, navigationalabilities, animal artificial language and cognitionprojects, Theory of Mind, and deception. Laboratoryexperimentalists and field scientists can be at odds,with those who have restricted their experience tothe laboratory to tend toward much more minimalinterpretations of animal achievements (as in animalculture)160 than would most ethologists.161

CONCLUSION

Over the last decade, there has been enormousinterest in and research relevant to CognitiveEthology, the field begun by Donald R. Griffin.Given the evidence, perhaps particularly that fromnonintrusive techniques finding similar brain activitiesand correlated behaviors in human and other species,a scientist is hard put to deny at least some levelof consciousness to nonhuman animals or to claimthat it is not a subject for scientific study. In 2012,prominent neuroscientists signed the CambridgeDeclaration on Consciousness asserting that evidencecould not support humans as the unique harbors ofconsciousness. The questions become which animalsare conscious, to what levels, and what best ways toinvestigate the phenomena.

It is also clear that exceptional intelligences mayexist for different species only in particular modulardomains, as driven by ecological and social factorsimpacting on their evolution. Advanced cognitiveabilities have been found in diverse species, includingthose with vastly different neural organization suchas the octopus, an organism deserving of furtherstudy. Some species exhibit episodic-like memory,

usually considered to be uniquely human; a strongcase is made from caching abilities of some corvids.Natural animal communication studies have revealedinformation within some signals that appears todesignate specific predator and predator classes andalso descriptors such as size, shape, color, and apotential predator’s speed and behavior, some ofwhich, however, may simply be correlates of urgency.Research has concentrated on vocal alarm calls,and should be extended to the more difficult taskof understanding communication not affording suchconspicuous responses to signals. Animals, often,but not exclusively, the great apes and corvids,have shown remarkable instances of problem solvingand novel tool creation and use, both in the fieldand in controlled captive conditions. The studyof behavioral strategies utilized in anti-predatoractivities has benefited from taking an intentionalstance, thereby generating hypotheses and detaileddata collection not typically gathered; the Pipingplover’s use of the broken-wing display is anexample. A burgeoning field of investigation intothe evolutionary origins of human senses of justiceand morality has shown widespread instances ofconcern for ‘fairness’ and ‘inequity aversion’ in thespecies studied, but should be extended beyondprimates and dogs. The behavioral expression ofsuch concerns depends on many factors, particularlysocial bonding strength and likelihood of a continuingrelationship; the field is not without controversy.And controversy still exists over the definitionsof many abilities, particularly as they relate tohuman abilities; examples include consciousness itself,episodic memory in animals, tool use, deception,and morality, among others. However, we shouldattempt to understand those capacities in relationto the organism’s particular ecological and socialneeds, not merely defining them in terms of humancapacities.

Varied research efforts have underscored theimportance of careful, detailed observations byexperienced researchers of animals behaving in theirnatural environments. From these can arise thehypotheses to be further investigated by additionalobservations and field and laboratory experiments.When experiments in the lab contradict plausibleinterpretations of behavior observed in the wild,scientists must be wary. The laboratory is ahighly circumscribed situation; experimental designshould allow for possible advanced capabilitiesto be demonstrated. We need to be aware ofpossible unrecognized assumptions about an animal’sperceptions and goals. We must realize possibleimpacts of boredom, of fear, of the salience of



the organism’s sensory system. In the end, in thebeginning, we must return again to von Uexkull’s

admonitions to be mindful of the Umwelt of theanimals we wish to understand.

ACKNOWLEDGMENTS

I thank Donald R Griffin for his continued inspiration; he would have been pleased to witness the burgeoninginterest and advances in fields in and related to Cognitive Ethology. I also thank W. John Smith, ConSlobodchikoff and Marta B. Manser for helpful discussions and/or manuscripts, as well as the WIREs editorsand staff, including Luca Tommasi for useful suggestions and Julie L. Nash for general assistance. I gratefullyacknowledge 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.


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Cognitive ethology