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CHAPTER Convergent Evolution of Cognition 5 in Corvids, Apes and Other Animals

Jayden O. van Horik, Nicola S. Clayton, and Nathan J. Emery

Abstract Over the past 30 years, a cognitive renaissance has produced startling revelations about how species perceive their physical and social worlds. Once considered mere automata by Descartes, recent research supports claims that many animals possess advanced cognitive capacities (Shettleworth, 2010). Moreover, advanced cognition appears to have arisen across numerous species, many of which are distantly related, but which share a number of traits, such as large relative brain size, complex sociality and behavioral fl exibility. Is the evolution of advanced cognition the result of a series of adaptive specializations driven by the shared selection pressures that species face in their environments? With our ex- panding awareness of cognitive processes across species, attributes such as causal reasoning, mental time travel or mental attribution, once thought unique to humans, invite careful reconsideration of their evolutionary origins. Key Words: behavioral fl exibility, convergent evolution, relative brain size, sociality, tool use

Introduction can be shared among distantly related species that Our understanding of the convergent evolution of face similar socio-ecological challenges. As a result, cognition hinges on comparative studies among analogous adaptations may evolve independently phylogenetically distinct species. Th is is not to say among distantly related organisms (Keeton & that comparative cognition is solely restricted to Gould, 1986). Any similarities in traits (i.e., cog- studies of distantly related species; comparisons nitive abilities) can then be attributed to shared between closely related species, such as humans and environmental selection pressures rather than to other primates, especially chimpanzees, also reveal characteristics present in a common ancestor (Ridley, compelling insights into the divergent processes of 1993). Consequently, the greater the phylogenetic cognitive evolution (e.g., Tomasello & Call, 1997). separation between groups, the stronger the case for However, the defi ning criterion of convergent evolu- evolutionary convergence (Papini, 2002). tion is that it occurs across distantly related species. One example of convergent evolution is the adap- As a result, the convergent evolution of adaptive tation of active fl ight among distantly related verte- traits can be considered to arise independent of brate species (Seed, Emery, & Clayton 2009). Birds, phylogeny shaped by common solutions to similar bats, and pterosaurs, for example, share the func- socio-ecological problems. tional ability of fl ight, but lack structural similarities By considering cognition as an adaptive special- in their forelimb morphologies (Figure 5.1). Flight ization—that is, a trait that is driven by environ- in birds evolved through the extension of the bones mental selection pressures—such selection pressures of the forelimb, whereas bats and pterosaurs support

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fact, governed by so-called higher-order cognitive processes, or whether intelligent behavior is simply the result of “hardwired” adaptive specializations— conserved associative learning processes (i.e., con- Pterodactyl ditioning). It is, therefore, important that cognitive processes are tested by determining whether certain behaviors can be fl exibly expressed across a variety of tasks of general equivalence.

Bird Comparing Intangible Traits & Inferring Tangible Proxies Unlike wings, which can be easily dissected to reveal any structural diff erences in morphology, cognition is an intangible trait ascribed to an organism’s psy- chology. Th us, comparisons may be made across Bat species only by identifying measurable proxies that are ecologically relevant to cognitive aptitude, such as measures of relative brain size.

Brain Structure and Function One useful proxy for intelligence is the size of spe- Human cifi c components of an organism’s brain relative to its overall body mass (Figure 5.2). Overall brain size has been criticized as a poor measure of cogni- Figure 5.1 Convergent evolution of wing and arm structure in tive capacity, because (1) brain size correlates with pterodactyls, birds, bats, and humans. Although the structure of the wing is diff erent in pterodactyls, birds and bats, the resultant body size, and (2) many brain areas control primary, behavior—fl ight—is the same. Th is may represent a parallel to sensory, and motor functions that are not directly convergent evolution of cognition in corvids and apes, yet with associated with cognition (Jerison, 1973). However, very diff erently structured brains. more recent studies have found that overall brain size is a better predictor of general intelligence (at the wing through extended digits: the fi fth digit for least in primates) than other measures, including pterosaurs; and the second, third, fourth, and fi fth relative brain size and neocortex size (Deaner, Isler, for bats. Yet, the convergent shape of the wing is the Burkart, & van Schaik, 2007). Yet there are certain result of environmental selection pressures and the areas of the brain that are more closely associated functional constraints imposed by fl ight. with higher-order processing, such as the neocortex Cognition has been described as “the mecha- in mammals and the forebrain in birds (Striedter, nisms by which animals acquire, process, store 2005). and act upon information from the environment” Jerison (1973) fi rst proposed an index to rank (Shettleworth, 2010, p. 4). Th is chapter proposes the cognitive skills of species based on their rela- a model of cognition as a domain-specifi c adaptive tive brain size, called encephalization quotient response to specifi c environmental selection pres- (EQ). Although there are obvious diffi culties in sures, which can then be generalized and applied making generalized comparisons across taxa that to solve novel tasks of functional equivalence. Th is live in diff erent environments, Jerison identifi ed proposal predicts diff erences between species based that some species are endowed with an exception- on diff erent levels and types of problem solving in ally high EQ and, hence, a relative brain size that is the wild. An alternative hypothesis proposes that much larger than would be predicted for their body there are no qualitative diff erences in the processes mass (Jerison, 1973). Of particular interest was the of cognition between species (Bolhuis & Macphail, fi nding that the relative size of the forebrain in cor- 2001), even in those that live in diff erent environ- vids (crows, rooks, and jays) and parrots is signifi - ments. We fi nd no evidence to support this alterna- cantly larger than those of other birds (cf. Emery & tive hypothesis. Clayton, 2004a). Corvids and parrots, in fact, pos- In addition to such mechanistic controversies is sess brains that are relatively the same size as those the debate about whether certain behaviors are, in of the great apes, and in both cases they are much

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Figure 5.2 Graph of log brain 3.5 volume against log body weight for a Dolphin Human number of birds (corvids, parrots, and 3 pigeons), mammals (rats, primates, Australopithecus cetaceans), Australopithecus and Homo Apes sapiens. Data on body size and brain 2.5 volume were taken from various published sources. 2

1.5 Parrots

log brain volume Other Birds 1 & Mammals Carvids Western 0.5 Scrub-Jay Pigeon Rat

0 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 log body weight

larger than predicted for their body mass (Jerison, brain, for example, it is the neocortex that mediates 1973). Although the issue of whether brain size cognitive processes (memory, reasoning, concept refl ects cognitive competence remains controversial formation, and social intelligence). However, birds (Striedter, 2005), it is clear that those avian species do not possess a neocortex. Measures of higher cog- that have relatively large brains, such as corvids and nition, such as foraging innovation and tool use are, parrots, also display cognitive abilities that have instead, identifi ed with certain areas of the avian hitherto only been demonstrated in large-brained forebrain (Lefebvre, Nikolakakis, & Boire, 2002), mammals (primates, cetaceans, elephants), espe- with areas analogous to the mammalian prefrontal cially those with a large prefrontal cortex (Emery & cortex, such as the nidopallium and mesopallium Clayton, 2004b; see later). (Reineret al., 2004; Rehkamper, Frahm, & Zilles, Th e common ancestor of birds and mammals, 1991). a stem amniote, lived over 300 million years ago. Although there may be fundamental diff erences During the course of such long independent in the size and structure of avian and mammalian evolutionary trajectories, corvids, parrots, and brains, recent evidence suggests that both groups apes adapted to radically diff erent environmental share advanced cognitive abilities (Emery, 2004). requirements (arboreal and terrestrial, respectively), Pepperberg (1999) provides a helpful analogy: “the but with shared or similar life histories (relatively structural diff erences between mammalian and avian long developmental period before independence, brains are like the wiring and processing diff erences great longevity, etc.), morphological adaptations between IBM-PCs and Apple Macs. However, in both (color vision, ability to track moving objects, fi ne cases, the resulting output (i.e. behavior or algorith- object manipulation, etc.), and socio-ecological mic operations) is similar.” Such similarities in cog- traits (omnivory, complex social groups, individual- nitive traits suggest that corvid and ape cognition ized relationships, etc.). has undergone a convergent evolution of mental Evolutionary divergence has resulted in the processes (Emery, 2004, Emery & Clayton, 2004b, independent evolution of diff erent neuroana- Seed et al., 2009). In fact, many animals demon- tomical components and structures across species. strate intelligent behavior, suggesting that cognition Mammalian brains, for example, are comprised of may have evolved independently among several diff erent components to those of birds, and they are vertebrate groups, including great apes (Tomasello organized into a laminar arrangement of neurons & Call, 1997), corvids (Emery, 2004), cetaceans compared to the nuclear clusters of neurons found in (Marino, 2002), hyaenas (Holekamp, Sakai, & avian brains (Emery, 2006). Yet analogous functions Lundrigan, 2007) and canids (Miklosi, Topal, & of particular brain components have been identi- Csanyi, 2004, Hare & Tomasello, 2005), among fi ed between these two groups. In the mammalian others (see later).

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Is Cognition Similar in Diff erent Species? be subjected to tighter energetic constraints and, Not only do corvids and apes appear to possess anal- thus, tend to possess signifi cantly smaller brains ogous neuroanatomical components responsible for than those of sedentary or nomadic species (Burish, cognitive processes, but they may also share similar- Kueh, & Wang, 2004). Th e occurrence of cognitive ities in how they form representations of their social traits may also be more likely to evolve among cer- and physical worlds. Th us, it is in the recognition of tain species. For example, the manufacture and use shared socio-ecological challenges that species face of tools is more frequently observed in great apes in their day-to-day lives that convergent adaptations than in birds. Th is may be because birds possess a may be revealed. For example, recent research has multifunctional beak, thus rendering the manufac- revealed evidence that corvids demonstrate similar ture of tools unnecessary in many of the foraging reasoning abilities as great apes, with regard to how challenges that birds encounter. tools work, how social agents can be manipulated, and how events are remembered (cf. Seed et al., Prerequsites for Intelligent Behaviour 2009). Cognition is thought to have arisen independently Recognizing behavioral similarities shared among across distantly related species through processes of diff erent species provides a basis for inferring simi- convergent evolution, driven by the need to solve larities in cognition. For example, using tools to comparable social and ecological problems (Emery aid in extractive foraging may not only be an adap- & Clayton, 2004a, 2004b; Marino, 2002; Seed, tive response to acquiring an otherwise inaccessible Emery, & Clayton, 2009). Such environmen- resource, but profi ciency might also be refi ned over tal challenges often require the ability to respond time through social learning. However, it is only by fl exibly by generalizing domain-specifi c behaviors going beyond the broad observations, such as that (i.e., behaviors evolved to solve specifi c problems), both apes and corvids are capable of tool manufac- and applying this knowledge to accommodate for ture, that information about how these species pro- more broad and variable interactions that species cess such information can be revealed. For instance, encounter in their environments. As a result, behav- what range of problems are these animals capable ioral fl exibility is often attributed as an indicator of of solving? Do they make or use tools for particular intelligence. purposes, adapting or modifying them depending Corvids have consistently demonstrated cog- on their context of use? Does a species’ understand- nitive skills that surpass those described in other ing of how tools work depend on causal reasoning birds, and in many cases they rival similar cognitive or other psychological processes? Only by conduct- domains previously thought confi ned to monkeys ing experiments using comparative methodology and apes (Emery, 2004; Emery & Clayton, 2004a, can we explain limits to such similarities and thus 2004b, Seed, Emery, & Clayton, 2009). Similarities establish the convergent processes of cognitive among species’ life history traits may, therefore, pro- evolution. vide clues to cognitive aptitude. Corvids and parrots Species with dramatically diff erent life histo- share with the great apes, many of the biological, ries, morphologies, brain structures, and ecologies ecological, behavioral, and psychological attributes may perceive the world quite diff erently from one thought fundamental to complex cognition. Each another. For this reason, it is important to consider of these aspects will be discussed in the following the ecological validity of comparative tests. Attempts sections outlining any similarities and discrepan- to make direct comparisons of psychological pro- cies between groups. Both corvids and parrots, cesses across phylogenetically distinct species may for example, possess forebrains that are relatively be marred by species-specifi c diff erences in percep- the same size as apes; experience a long develop- tion, attention, and motivation (Bitterman, 1960, mental period before becoming independent from 1965). their parents; are long-lived, omnivorous extrac- An organism’s neuroarchitecture is infl uenced tive foragers; and live in complex social groups—all by adaptations to specifi c environmental selection socio-ecological attributes that have long been sug- pressures. For instance, there may be diff erences in gested as prerequisites for intelligence in primates the environmental constraints imposed on brain size (Byrne & Whiten, 1988; Humphrey, 1976). among aquatic species compared with aerial spe- It is likely that each of the socio-ecological attri- cies. Moreover, species’ life histories may also result butes described later corresponds with diff erences in in more subtle variations. For example, migratory domain-specifi c cognitive abilities. Chimpanzees, birds that spend much of their life in fl ight may for example, use tools more frequently than their

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closely related cousins, bonobos, and, hence, possess with substantial increases in brain size in the post- a more sophisticated understanding of physical cau- natal period. Indeed, there is also a clear relation- sality or “folk physics” (Herrmann, Hare, Call, & ship between length of juvenile period (and age Tomasello, 2010). Yet, those species with the most at maturation) and relative brain size in primates advanced cognitive abilities are likely to incorpo- (Ross, 2004). rate a number of these socio-ecological attributes Relatively extended periods of juvenile develop- (Emery, 2006), although the question that remains ment may serve to accommodate the acquisition of to be answered is to what degree these socio-ecolog- knowledge, either by social learning from adults to ical pressures correlate with cognitive fl exibility and off spring or individual learning based on trial-and- how these pressures are refl ected in the underlying error. Although this hypothesis is attractive, there cognitive systems of animals, which we are still far is little data to support such a claim. Indeed, there from knowing. is no correlation between environmental complex- ity (social, physical, dietary, ecological, and climatic Biological Similarities uncertainty) and brain size in primates when con- In this section, we highlight a number of shared bio- trolling for postnatal growth rates in primates (Ross, logical features found in corvids, parrots, and apes, 2004), and the developmental period of corvids and however, we are aware that these are general claims parrots is relatively long compared to other birds, and that some of the traits are shared with other but relatively short compared to apes (Iwaniuk & animals. Th e function of this section is to highlight Nelson, 2003). In addition, a species’ lifespan may those features that are shared by these taxonomic also infl uence its cognitive capacity because long- groups and may contribute to the similarities in lived individuals may accumulate knowledge and behavior and cognition we will describe in later experience and use such knowledge to make better sections. decisions and be better prepared to solve and adapt to future problems. parenting, development, and lifespan Ontological diff erences among species reveal impor- dexterity tant trends in the evolution of relative brain size, Species equipped with grasping or dexterous limbs particularly between altricial and precocial species. (primates) or generalized all-purpose beaks (birds) Altricial species are born into the world blind, help- may be better equipped to solve physical tasks less, and utterly dependent on parental care. Yet than those species that cannot easily manipulate precocial species are immediately capable of surviv- objects. Parrots, for example have particularly dex- ing independently. Such stark diff erences in juvenile terous grasping feet, which they eff ectively use to development may appear at odds with initial sur- manipulate food. Similarly, primates possess hands vival success, yet they foretell strategic diff erences in and feet that can be used to manipulate objects. species’ life histories. Corvids tend to use their beaks as tools, suitable for In birds, altricial hatchlings possess signifi cantly prying open, digging, puncturing, and crushing a smaller brains relative to their body size than preco- variety of food sources, as well as a number of fi ne cial hatchlings (Bennett & Harvey, 1985). However, manipulations. Such a number of fl exible move- altricial adult birds possess signifi cantly larger brains ments allow these groups to exploit objects in their relative to their body size than precocial adult birds environment unavailable to other groups, which in (Starck, 1993; Starck & Ricklefs, 1998). Th ese fi nd- turn require additional levels of neural and cogni- ings suggest that the majority of neural development tive processing power not seen in other species with- occurs in birds during an extended posthatch- out such dexterity. ing period, rather than during incubatory peri- ods. However, prolonged periods of development, visual acuity whether during the incubatory period or posthatch- Among primates, brain size is positively correlated ing period, are, in fact, correlated with increases with visual specialization (Barton, 1998). In fact, in relative brain size (Iwaniuk & Nelson, 2003). the primate neocortex is comprised of about 50 Th us, extended developmental periods and longer percent of visual areas, allowing for accurate and durations of parental care correlate positively with high-resolution processing (Van Essen, Anderson, relative brain size (Ricklefs, 2004). A similar picture & Felleman, 1992). High visual acuity may be par- emerges for the great apes. Apes are also an altri- ticularly benefi cial to primates and birds because it cial species, displaying a slow rate of development, may enhance their ability to detect ripe fruits and

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moving insects, as well as predators. Th e relatively same point in evolutionary time (5–10 million years large brains of frugivorous primates, as opposed to ago) during the Late Miocene and Pliocene epochs folivorous species (Clutton-Brock & Harvey, 1980), (Emery, 2006; Potts, 2004). Th is period is char- may thus have resulted from selection pressures act- acterized by dramatic environmental and climatic ing to enhance the detection of edible fruits using variability and instability as a result of numerous specifi c visual cues such as color. In addition, visual ice ages. Such environmental changes would have acuity may allow for the detection of social informa- strongly infl uenced food availability and conse- tion, such as facial expressions and the gaze direction quently species’ foraging strategies. of conspecifi cs (Barton, 1996). Th us, it is not sur- During evolutionary history, the abundance of prising that there is a strong relationship between the resources may have fl uctuated, becoming less reli- size of the visual system and socio-ecological vari- able and irregularly distributed through time and ables such as diet and social group size in primates. space. Food scarcity may have been alleviated by Unfortunately, comparable data do not exist the evolution of foraging techniques to exploit new for birds. However, birds are highly visual animals resources. However, species that are governed by (Hodos, 1993), processing color information in a rigid stimulus-response action patterns or hardwired greater frequency range than mammals (including behaviors may not respond as well to such changes ultraviolet), as well as rapidly processing move- as those species that adopt fl exible behaviors based ment information. Th e eyes of birds and mammals on more abstract knowledge (Seed et al., 2009). As are quite diff erent, yet the central neural systems such, extracting food hidden within encased sub- are relatively similar (Husband & Shimizu, 2001). strates or procuring meat as an energy-rich food We may, therefore, predict a similar relationship source may have become incorporated into species’ between the visual system and socio-ecological vari- foraging repertoires. Th us, environmental variabil- ables in birds. Indeed, in the case of prey capture, ity may have selected for certain species to adopt there is a co-evolutionary relationship between eye innovative, omnivorous, and generalist foraging size and brain size (Garamszegi, Moller, & Erritzoe, techniques, powered by increases in relative brain 2002). size (Lefebvre, Reader, & Sol, 2004). Such eco- logical variables have been suggested as important brain size evolutionary drivers of great-ape cognition (Potts, Th e relative size of corvid, parrot, and ape brains are 2004); similar conditions may also be responsible equivalent in terms of brain size to body size (i.e., for the evolution of avian (corvid and parrot) cogni- are found on the same regression line; Emery and tion (Emery, 2006), as well as other species living Clayton, 2004b). An enlarged brain is metabolically in such changeable environments, such as cetaceans expensive (Aiello & Wheeler, 1995). Th us, it is gen- (Marino et al., 2007) and elephants (Byrne & Bates, erally accepted that there must be correspondingly 2009). powerful adaptive benefi ts from brain enlargement. One important feature of an unpredictable Understanding the origins of this specialization, environment is the source of food. Foods that are therefore, becomes a question of what selective ephemeral, that have to be hunted, that appear at pressure(s) favored enlarged components of the certain times of the year, that are distributed in brain during the course of evolution (Isler & Van clumps or need to be extracted from casings, will Schaik, 2009). require more cognitive abilities to obtain (e.g., spa- As discussed earlier, the relative size of specifi c tial memory, planning, cooperation) than foods that components of an organism’s brain can be used as a are available all year, located in the same place, and direct proxy to inferring higher cognitive facilities. which require little processing, such as foliage. However, it is important to recognize that any inter- pretations must be made with caution, because dif- generalized diet ferent assumptions and methodological approaches Many corvids, parrots, and primates are omnivo- can easily distort species-wide comparisons (see rous, generalist foragers. Rooks, in particular, Healy & Rowe, 2007). consume over 170 species of plants and animals, including many diff erent parts of plants, insects, Ecological Similarities worms, seafood, birds’ eggs, small vertebrates, and unpredictable environments carrion (Cramp & Perrins, 1994). However, rooks Th e most recently evolved genera of corvids (Corvus, acquire the majority of their diet through extractive Pyrrhocorax) and apes (Pan) appeared at roughly the foraging techniques; digging in the soil for grain,

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invertebrates, roots, and tubers (Lockie, 1955). and dexterity to succeed. Chimpanzee infants Some corvids also use their beaks to hammer and require years of observation to learn how to make pry open the hard cases of nuts such as walnuts and tools (Biro et al., 2003; Lonsdorf, 2006). Similarly, acorns, and drop mussels, limpets, and bone from capuchins’ success at nut cracking varies consider- the air until their encased contents are released. ably between individuals and is likely to require Parrots also consume a wide variety of seeds, years of practice to attain an effi cient technique fruits, and fl owers (Juniper & Parr, 2003). Some (Fragaszy et al., 2010). species, such as the kaka frequently consume insects Extractive foraging may have evolved in response (Moorhouse, 1997), use their large, down-curved to food scarcity. Species that evolve novel foraging bills to tap sap from trees and excavate grubs from techniques may exploit niches that are not readily both live and dead wood (Beggs & Wilson, 1987). available to others, often containing energy-rich Another New Zealand parrot, the kea, renowned foods that are high in nutritive value and avail- for its extreme neophilia and advanced intellect able throughout the year. In addition, extracting (Huber & Gajdon, 2006), is also known to con- encased foods often requires a variety of complex sume a varied diet, including over 40 plant species sensorimotor skills for locating and manipulating (Clark, 1970) as well as discarded fat, protein, and food items. Such processes have been suggested to carbohydrate-rich foods found in human settlements provide support for the evolution of intelligence (Diamond & Bond, 1999; Gajdon, Fijn, & Huber, in apes (Parker & Gibson, 1977), although other 2006). Th e kea is also notable as the only carnivo- studies on primates found no relationship between rous parrot known for attacking sheep and eating fat extractive foraging and neocortex ratio (Dunbar, from the back of the animal (Benham, 1906; 1995). Diamond & Bond, 1999), as well as excavating sooty shearwater chicks from their underground nest foraging in space and time burrows (Cuthbert, 2003). Utilizing such a vari- Th e main foods consumed by corvids, parrots, and ety of food sources is a likely response to living in primates (fruits, seeds, and invertebrates) are often mountainous regions characterized by a harsh and patchily distributed through space and vary in their unpredictable climate, resulting in an irregular food temporal availability. Other species may also face supply. It is not yet clear whether the seemingly similar challenges in locating food items, such as more complex dietary habits of keas, when com- cetaceans’ diet of fi sh, krill, and cephalopods, which pared to other parrots, is refl ected in their physical may be equally variable in abundance and distri- cognition (Liedtke, Werdenich, Gajdon, Huber, & bution (Marino, 2002). However, such temporal Wanker, 2010). and spatial patchiness may be predictable; plants Seeds are a more common component of parrots’ remain in the same place and fruits often ripen at diets, but many seeds have a hard case, requiring predictable intervals. Likewise, regularities in ocean dexterous manipulation to extract their contents, currents or seasonal spawning times may allow ceta- preventing most other arboreal foragers access. ceans to predict the location and timing of abun- Yet some parrots, for example, hyacinth macaws dant food supplies. (Borsari & Ottoni, 2005) and black palm cockatoos Yet closely related species can diff er substantially (Wallace, 2000), profi ciently open hard-cased seeds in their dietary requirements and hence forag- by using wedgelike pieces of wood or leaves as tools ing strategies. Some primates rely on a varied diet to better grip nuts with their upper mandible, and, of fruits, whereas others predominantly consume while holding the nut in place with one foot, open leaves. Leaves are, however, considerably more the hard casing with their lower mandible. abundant than fruits, and their distribution is regu- Primates also demonstrate skillful extractive lar. Frugivorous primates are, therefore, faced with foraging techniques, the most prominent example an additional challenge; locating an ephemeral and being termite fi shing by wild chimpanzees (Goodall, patchily distributed resource. However, primates 1963; van Lawick-Goodall, 1968). However, chim- that remember the locations and fruiting patterns panzees (Boesch & Boesch, 1990) and capuchins of a variety of plant foods might improve their for- (Fragaszy, Izar, Visalberghi, Ottoni, & de Oliveira, aging effi ciency (Janmaat, Byrne, & Zuberbuhler, 2004) also crack hard- cased nuts with hammers 2006). Selection pressures, favoring foraging effi - and anvils to extract their contents. Although such ciency, are, therefore, thought to enhance species’ behaviors are commonly observed, termite fi shing cognitive capacities for spatial and temporal mem- and nut cracking require sophisticated manipulation ory (Milton, 1981). As such, cerebral expansion is

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more pronounced in frugivorous primates, rather as a means to extend the physical infl uence realized than folivorous species (Clutton-Brock & Harvey, by the animal” (Jones & Kamil, 1973, p. 1076). 1980). Hence, vultures that crack open eggs by dropping Some animals have evolved specializations them onto rocks do not demonstrate tool use, for remembering and predicting the location of whereas vultures that throw stones (as a physical resources that are irregularly distributed through extension of their body) to open eggs fi t these cri- time and space. Th e most extensively documented teria. Likewise, the examples of corvids dropping accounts of such behavior come from experiments mussels to crack open their hard shells, thrushes on spatial memory in food-caching animals (Vander that open snail shells by smashing them onto stones Wall, 1990). When an abundant food supply is (Gibson, 1986), or crows in Japan and California available, many animals store food for consumption that open hard-shelled walnuts by dropping them in later periods of food scarcity. However, to effi - from great heights onto hard-surfaced roads (Cristol ciently recover their caches, storers need to process and Switzer, 1999; Nikei, 1995) do not demonstrate information relating to the location of their cache tool use when discussed in terms of the earlier defi ni- sites, the type, and perishability of stored food tion. However, manipulating encased food items to items, and the social context of caching (Clayton & extract their contents (extractive foraging) requires Dickinson, 1999; Clayton, Dally, & Emery, 2007; certain forms of cognition, particularly when com- van Horik & Burns, 2007). Some corvids, such as pared with nonextractive forms of foraging. Clark’s nutcrackers, can cache up to 30,000 pine Although most species of great apes make and seeds over large areas, recovering a majority of them use tools, the most profi cient primate tool user in up to six months later. Such behaviors suggest that the animal kingdom is the chimpanzee (Tomasello these birds possess a profi cient long-term spatial & Call, 1997). Yet there have also been numer- memory (Balda & Kamil, 1992). Conversely, other ous reports of tool use in birds, especially corvids corvids, such as Western scrub jays, cache fewer (Lefebvre et al., 2002). One of the most strik- but a wider variety of food items that diff er in ing applications of tool use by any animal can be their rates of perishability. Consequently, Western observed in wild New Caledonian crows. Th ese scrub jays not only remember where they cached, birds routinely use and transport manufactured but also what they cached and when, so that per- tools during daily foraging expeditions, and they ishable food can be recovered when it is still edible use diff erent types of tools depending on their func- (Clayton & Dickinson, 1998, 1999; Clayton, Yu, tional requirements: stepped-cut Pandanus leaves & Dickinson, 2001, 2003; de Kort, Dickinson, & are used in a rapid back and forth fashion to search Clayton, 2005). for prey under leaf litter, whereas hooked twigs are used to extract insect larvae from within tree cavities Behavioral Similarities using slow deliberate movements (Hunt, 1996). tool use and manufacture Both New Caledonian crows and chimpanzees Recently thought to be uniquely human, the fi rst manufacture tools, either fashioning probing sticks report of tool use outside of humans was in wild by stripping off smaller twigs and leaves from larger chimpanzees (van Lawick-Goodall, 1968). We now twigs and then inserting them into termite mounds, know that many species of insects, fi sh, birds, and making hook tools by removing a series of side mammals use tools in the wild (Beck, 1980; Emery twigs from a larger twig and then chiseling away at & Clayton, 2009b). However, in the wild, only a breakage point to create a hook, or cutting steps chimpanzees, orangutans, New Caledonian crows, into a pandanus leaf to make a pointed and rigid and woodpecker fi nches habitually use and manu- tool for rooting out grubs living under the bark of facture tools during their daily foraging activities dead trees (Sanz, Call, & Morgan, 2009; Hunt & (Hunt, 1996; Tebbich, Taborsky, Fessl, & Dvorak, Gray, 2004; Hunt, Corballis, & Gray, 2006). In 2002; Tomasello & Call, 1997; van Schaik et al., all these cases (and others not described here), the 2003). Yet the extent to which these animals under- toolmaker starts to create a tool from raw material stand how tools work, that is, their physical proper- (twigs, leaves, etc.) by removing or sculpting parts of ties and the unobservable forces that govern their the raw material that is nonfunctional as a tool, into function—so-called folk physics—remains contro- a functional tool. Although we know little about the versial (Emery & Clayton, 2009b; Povinelli, 2000). psychology of toolmaking, this ability suggests that Tool use requires “the use of physical objects the toolmaker may have an image of the fi nal tool in other than the animal’s own body or appendages mind before it is made.

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sociality largest relative brain sizes are found among long- Observations of social interactions among captive term monogamous species and cooperative breeders chimpanzees fi rst prompted the hypothesis that (Emery, Clayton, et al., 2007). social living and, thus, the challenges that species Species that live within fi ssion-fusion societies face in their social environment play important are presented with the additional cognitive chal- roles in the evolution of a fl exible and intelligent lenge of adjusting to dynamic social changes, result- mind (Social Intelligence Hypothesis: Humphry, ing from the movement of numerous individuals 1976). Th is hypothesis was later recognized as a into and out of groups at various times (Aureli key component of primate cognition, attributing et al., 2008). Rooks, for example, congregate in large social intelligence to the recognition and subse- colonies during the breeding season; then, after they quent manipulation, coordination, and deception have raised their off spring, each breeding pair will of individuals within a social group (Machiavellian disperse to form smaller foraging groups. Similar Intelligence Hypothesis: Byrne & Whiten, 1988). social structures are exhibited across a number of Further support for these theories was later found in distantly related species that demonstrate high levels positive correlations between social-group size and of sociality and social complexity such as chimpan- neocortex size in primates (Social Brain Hypoth- zees (Goodall, 1986), cetaceans (Connor, Mann, esis: Dunbar, 1998, chapter 6 of this volume), and Tyack, & Whitehead, 1998; Marino, 2002; Smolker, cetaceans (Marino, 1996). Th e rationale behind Richards, Connor, & Pepper,1992), and possibly these theories is that selection favors those animals some corvids (Emery, 2004). that profi ciently keep track of the identities and interactions of numerous individuals within large relationships social groups. Over evolutionary time, this process Many animals not only recognize individuals resulted in the refi nement of social cognition as an within a group but also understand intragroup rela- adaptive specialization. tionships, such as kinship and the social status of Although there appears to be a clear indication individuals relative to other group members (e.g., that group size has played a signifi cant role in the dominance rank). Such interactions become par- evolution of brain size in primates, similar relation- ticularly clear during disputes over food or mates. ships are not shared among birds (Emery, Seed, von During disputes, animals may recruit support from Bayern, & Clayton, 2007). Such diff erences may, bystanders or relatives to form alliances; however, therefore, be attributed to the structure of social supporting a loser may prove costly. Th erefore, it groups. For example, primates form polygynous pays to recruit and support high-ranking individuals social groups, whereas birds are often monogamous, as well as consider the strength of preexisting intra- forming life-long pair bonds. Moreover, group size group alliances. Making such decisions relies on in primates may be relatively stable, yet there can be the possession of a detailed understanding of third- considerable seasonal variation in birds’ fl ock size. party relationships (Schino, Tiddi, & Di Sorren- Similar correlations between relative brain size and tino, 2006; Silk, 1999), however, heuristics such as certain aspects of sociality have, however, been iden- “always recruit the most dominant animal” may also tifi ed in some avian species such as corvids (Emery, explain behavior consistent with that of third-party Clayton, & Frith, 2007). Social intelligence in birds recognition (Range & Noe, 2005). may have thus evolved in response to the require- Until recently, third-party relationships were ments of maintaining relationships and coordinat- considered a unique attribute of primate cogni- ing cooperative behavior within monogamous pairs, tion (Tomasello & Call, 1997). However, many rather than having been driven by the need to man- mammals, such as elephants, whales, dolphins, and age competitive interactions imposed by group liv- hyenas, form long-lasting groups that are comprised ing as in primates. In other words, it may be the of similar kin and dominance networks to those of quality rather than the quantity of relationships that primates (Connor, 2007; de Waal & Tyack, 2003; are important for birds (Emery, Seed, et al., 2007). Holekamp et al., 2007). Like primates, hyenas sup- In socially monogamous birds, an increase in the port conspecifi cs engaged in agonistic interactions. quality of parental care may lead to increasing pay- Engh and colleagues (Engh, Siebert, Greenberg, & off s; more experienced pairs (those that have paired Holekamp, 2005) observed that in most disputes, for more than one breeding season) may raise more the aggressor was the more dominant individual. As chicks. As such, comparisons between brain size such, support from conspecifi cs was usually directed and mating system in birds have revealed that the toward the more dominant individual, possibly

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confi rming a “join the aggressor” rule of thumb, Cooperative coalitions are often observed in rather than specifi c knowledge of an individual’s many social species. Female primates and ceta- relative rank. However, in a minority of cases, when ceans for instance, demonstrate alloparental care— a subordinate attacked the dominant, joiners also “babysitting” or staying within close proximity to supported the dominant, suggesting knowledge unrelated juveniles (Marino, 2002; Nicolson, 1986). of the relative rank of each individual (Engh et al., Chimpanzees (Uehara, 1997), bonobos (Hohmann 2005). & Fruth, 2008), whales (Hain, Carter, Kraus, After disputes, hyenas (Engh et al., 2005) and Mayo, & Winn, 1982; Jurasz & Jurasz, 1979), and primates (Tomasello & Call, 1997) are more likely dolphins (Leatherwood, 1975; Wursig & Wursig, to redirect their aggression toward relatives of a 1980) all exhibit cooperative feeding strategies that former opponent rather than other low-ranking require coordinated eff orts of individuals within a individuals. Th is suggests a knowledge of kin- group to capture prey. Male chimpanzees (Watts, ship, dominance, and third-party relationships. 1998; Wrangham, 1999) and bottlenose dolphins However, these fi ndings may be biased because of (Connor, Smolker, & Richards, 1992) also form close proximity of relatives and hence increased cooperative alliances or coalitions for the purposes interactions. To further test this, Holekamp and of intergroup aggression (“warfare”) and mate colleagues (2007) played back distress calls of hyena guarding. Recently, brown-necked ravens have been pups and found that both mothers and nearby rela- shown to also use cooperative hunting, with indi- tives of the calling cubs were more likely to elicit a viduals taking diff erent roles when hunting large response than unrelated individuals. Moreover, the lizards (Yosef & Yosef, 2009). dominance rank of the mother also infl uenced the looking of others. Together, these results provide innovations support for kin, dominance, and third-party recog- To accommodate rapid changes in their environ- nition in hyenas. ment, some animals may behave fl exibly by adopt- Captive rooks and jackdaws also form long-term ing innovative techniques to solve novel problems. alliances with other group members, sometimes Overcoming such challenges may require species to irrespective of sex or kinship (Emery, Seed, et al., possess advanced cognitive mechanisms to process 2007). Relationships in young rooks and jackdaws and manipulate environmental information, result- are thought to be initiated by food sharing, dem- ing in enlarged components of the brain (Dunbar, onstrated by the unsolicited transfer of food from 1992). Comparing relative brain size with measures one individual to another (active giving; de Kort, of behavioral complexity across species has revealed Emery, & Clayton, 2003), which is considered an some of the most compelling evidence linking essential component of pair formation (von Bayern, the evolution of brain and cognition (Lefebvre, de Kort, Clayton, & Emery, 2007). Alliances in Whittle, Lascaris, & Finkelstein, 1997; Lefebvre corvids and apes are maintained through the use et al., 2004). of affi liative behaviors, such as allopreening and Ethologists have long observed the complex and grooming, respectively (de Waal & Lutrell, 1988; fl exible behaviors performed by animals in the wild, Emery, Seed, et al., 2007; Seyfarth & Cheney, documenting the emergence of novel behaviors and 1984). publishing anecdotal reports as short notes in scien- Rooks that form pairs enhance their individual tifi c journals. Reports of such innovations have been dominance rank compared to those that remain collated across numerous species and used to produce single (Emery, Seed, et al., 2007). Enhanced domi- measures of species’ behavioral plasticity (Lefebvre nance in turn provides associated benefi ts such as et al., 1997, 2004). Accounts of innovations, in terms increased food acquisition. Emery, Seed, and col- of their relative frequencies of occurrence (innova- leagues (2007) also report that rooks are sensitive tion rates), have been compared across species and to third-party relationships, as they redirect aggres- found to correlate positively with relative brain size sion to the partner of an individual that they have in birds and primates (Lefebvre et al., 1997, 2004), received aggression from. Furthermore, rooks with corvids, parrots, and apes at the forefront of engage in third-party affi liation with their partner innovative groups (Seed et al., 2009). Similar rela- (i.e., bill twining) after confl icts with other group tionships between the observed frequency of tool use members, however, unlike primates, they do not in birds and relative brain size have also been identi- reconcile with former opponents (Seed, Clayton, & fi ed (using the same method of collating anecdotes; Emery, 2007). Lefebvre et al., 2002). Likewise, the relative size of

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the “executive brain” (neocortex and striatum) in chimpanzees with two pieces of food placed in an primates has been found to correlate positively with arena; the subordinate chimp could see both pieces the number of reports of innovation and tool use in of food, whereas the dominant chimp could see primates (Reader & Laland, 2002). only one. Because dominant chimpanzees monopo- lize resources, the only way for the subordinate to Psychological Similarities gain any of the food was to obtain the food that social reasoning the dominant could not see. When released into Sociality is thought to have played an important the arena, subordinates typically adopted this strat- role in the evolution of intelligence (Byrne & egy, however, there are some discrepancies in the Whiten, 1988; Dunbar, 1998; Humphrey, 1976; interpretation of these results (see Karin-D’Arcy & Jolly, 1966). As such, individuals within a group Povinelli, 2002). may gain a competitive advantage (and fi tness ben- A series of controls that allowed subordinates a efi ts) through the use of social cognition (Humphry, head start in retrieving the food further revealed that 1976). It has, thus, been proposed that the recogni- subordinates were not responding to the approach tion of other group members as intentional agents, behavior or gaze direction of the dominants (Hare which possess individual beliefs and desires, inde- et al., 2000). Th is suggests that the subordinate’s pendent of one’s own, provide the basis for complex decision about which piece of food to obtain was social interactions (Tomasello & Call, 1997). dictated by their understanding of what the domi- Terms such as “chimpanzee politics” have been nant could or could not see. However, an alterna- used to describe the sophisticated social interactions tive explanation is that the subordinates based their of primates (de Waal, 1982), especially involving decision of where to forage on their memory of cooperation, alliance formation, social maneuver- where the dominant was looking before the barrier ing, manipulation, and deception. However, such was raised (i.e., where the dominant was looking complex “political” interactions may not be before they made an approach movement; Povinelli restricted to primates, because similar behaviors & Vonk, 2004). have also been observed in numerous species such In subsequent experiments, Hare and colleagues as corvids (Emery, Seed, et al., 2007), cetaceans (Hare, Call, & Tomasello, 2001) further investi- (Marino, 2002), and hyenas (Holekamp et al., gated what chimpanzees know about what others 2007). Evidence from such a wide variety of dis- know (i.e., what others have and have not seen in tantly related species further supports the theory of the immediate past), by manipulating (1) whether a an evolutionary convergence of social cognition. dominant individual could see where the food was One of the consequences of social living is that hidden, (2) misinforming the dominant’s knowl- individuals within a group are likely to forage in the edge, and (3) replacing informed dominants with same areas for the same resources, thus resulting in uninformed dominants. Th e fi ndings of this study direct competition. For instance, chimpanzees nat- suggest that chimpanzees can recall what another urally compete over food (Tomasello & Call, 1997), conspecifi c had and had not seen in the immediate although in certain circumstances food sharing does past, and attribute specifi c knowledge of events to occur: from mother to infant, or when close associ- particular individuals (Hare et al., 2001). Although ates share prey that cannot be monopolized by any widely cited, this study is not without its critics who one individual, such as a monkey killed during a suggest that the chimpanzees’ behavior does not cooperative hunt (Uehara, 1997). have to be the result of mental attribution; rather, Often resources may be irregularly distributed it only needs to be based on sophisticated behavior- and found in aggregated patches. Hence, when for- reading (Emery & Clayton, 2009a; Karin-D’Arcy & aging in a group, it may be advantageous for indi- Povinelli, 2002; Povinelli & Vonk, 2004). viduals to be vigilant of where other group members Other examples of conspecifi c perspective tak- are successfully locating food. Likewise, competition ing and knowledge attribution are illustrated in may pose risks of food theft or displacement from experiments on food-caching corvids. Many birds abundant food supplies by more dominant individ- and mammals hide food for future consumption uals. Th us, animals that know what conspecifi cs can (Vander Wall, 1990). However, storing food poses and cannot see may benefi t by using this knowledge the risk of theft, especially if the storer cannot in food competition situations. defend their caches. In species that forage in social Hare and colleagues (Hare, Call, Agnetta, & groups, theft from conspecifi cs may be particularly Tomasello, 2000) tested this theory by presenting accentuated. Corvids, for example, have an excellent

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observational spatial memory and observe one a of the same object. Th e extent to which nonhu- nother’s caching behavior to accurately locate oth- man species utilize gaze cues to locate food or infer ers’ stores and pilfer their contents at a later time mental states, rather than following gaze, is contro- (Bednekoff & Balda, 1996a, 1996b; Bugnyar & versial (Emery & Clayton, 2009a). It is clear that Kotrschal, 2002; Clayton et al., 2001), even if caches both corvids and apes follow the gazes of a human were made from a completely diff erent perspective experimenter, but they also reposition themselves (Watanabe & Clayton, 2007). As such, corvids have to follow the experimenter’s gaze around a visual evolved numerous strategies to reduce the probabil- barrier (Brauer, Call, & Tomasello, 2005; Bugnyar, ity of their caches being stolen by others (Dally, Stowe, & Heinrich, 2004; Schloegl, Kotrschal, & Clayton, & Emery, 2006). Corvids readily cache Bugnyar, 2007). in lab aviaries, basing their caching decisions on Another common paradigm to test whether ani- the presence or absence of conspecifi cs (Emery & mals understand that gaze cues can refer to objects Clayton, 2001). Under solitary conditions, birds outside of view is the object-choice task. In this do not apply cache-protection strategies. However, test, animals have to use experimenter-given social when conspecifi cs are present, birds attempt to cues, such as pointing and gaze, to locate food hid- reduce the amount of information available to den under one of two containers. Success varies observers by caching in places that are either dif- across species; apes often perform inconsistently fi cult for the observer to see (i.e., further away or (Call, Hare, & Tomasello, 1998; Call, Agnetta, & behind barriers; Dally, Emery, & Clayton, 2005) Tomasello, 2000), African grey parrots rapidly or where the information of cache location is visu- learn to attend to some experimenter cues, but in ally degraded (i.e., in dark places; Dally, Emery, most cases they did not do so spontaneously (Giret, & Clayton, 2004). Storers also move their caches Miklosi, Kreutzer, & Bovet, 2009), whereas jack- from locations observed by potential thieves to daws use cues that serve a communicative function places unbeknown to thieves, and they appreciate in humans (von Bayern & Emery, 2009). Perhaps that diff erent individuals have seen diff erent events. surprisingly, domesticated species, such as goats Whether these diff erences are based on diff erent and dogs, have had more success than primates knowledge states (i.e., knowledgeable or ignorant) (Hare, Brown, Williamson, & Tomasello, 2002; is debatable (Emery & Clayton, 2008). Similar Kaminski, Riedel, Call, & Tomasello, 2005, but see studies have also revealed that ravens can discrimi- Emery and Clayton, 2009a, Miklosi and Soproni, nate between human and conspecifi c competitors 2006). based on diff erences in the information they have been given access to (Bugnyar & Heinrich, 2005). tactical deception Although studies on cache-protection strategies in Species that forage in social groups share direct corvids reveal similar fi ndings to studies on food competition over access to resources. Selection is, competition in chimpanzees, both groups, for thus, thought to favor individuals that can mitigate example, appear to appreciate the perspectives of these costs by using social knowledge as a means others, and it remains unclear whether such fi nd- to employ socially manipulative tactics. Hence, the ings are based on reading the behavior of others or social intelligence, social brain, and Machiavellian reading their mental states. intelligence hypotheses, link the cognitive demands Th e strongest cue representing what others see of social living with the evolution of enhanced and where others are looking is the direction of their social skills and increases in brain size (Byrne and eye gaze. Perceiving such a cue may be particularly Whiten, 1988; Dunbar, 1998, 1992; Humphrey, valuable for social species with immediate adaptive 1976). benefi ts, such as locating food sources, predators, Tactical deception (TD) has been used to and mating partners. Although primatologists in describe how individuals psychologically manipu- the fi eld have long suspected that primates respond late the behavior of others within a social group to the presence of gaze cues in conspecifi cs (Emery, (Byrne & Whiten, 1985). Behaviors suggested to 2000), Emery and colleagues (Emery, Lorincz, represent such psychological manipulations have Perrett, Oram, & Baker, 1997) were the fi rst to been reported for numerous primate species, but experimentally test this behavior in the context they are anecdotal in nature and not replicable, so of gaze following. Th ey found that captive rhesus their utility as a source of information on social monkeys reliably followed the gaze direction of con- cognition is questionable (Whiten & Byrne, 1988). specifi cs toward target objects, ignoring distractors Interestingly, however, the number of records of

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tactical deception correlates signifi cantly with neo- an observer (Emery & Clayton, 2008). If jays had cortex size in primates (Byrne & Corp, 2004). Th is cached items in specifi c locations in front of a spe- relationship remains when group size is accounted cifi c observer and then retrieved these caches in front for, eliminating concerns that larger groups present of the same or a diff erent observer, they recovered more opportunities for deception. Furthermore, only those items that the observer had seen being this relationship is also consistent with the idea that cached and left the other unknown caches alone. cognitive problem solving is constrained by neo- Th e caches that were recovered tended to be moved cortex size, supporting the link between the evolu- around multiple times and were not necessarily left tion of the neocortex and increased complexity of in the last cache site that the jay made a bill probe social living (Byrne and Whiten, 1988; Dunbar, into (Dally, Emery, & Clayton, 2006). Th is suggests 1998; Humphrey, 1976). However, it is not clear that the caching jays may have been deceiving the whether such behaviors, if they exist, are unique to observers about the fi nal location of the cache. primates; comparable studies on other species have not focused on their intelligence in the wild. Studies physical reasoning on birds, for example, far exceed those on primates It is a long-held assumption that species that employ (certainly in terms of the number of observation the use of tools to aid in procuring food from inac- hours recorded and the number of species studied), cessible areas have greater intelligence, especially but no fi eld study has yet, to the best of our knowl- in terms of physical cognition, than those species edge, focused on questions of cognition (social or that do not use tools (Emery & Clayton, 2009b). physical). It is, therefore, less likely that such reports Although chimpanzees use a variety of tools in the of novel social behavior would be reported for wild, there is little evidence that they necessarily nonprimate species. understand how the tools that they use work (Pov- Th is does not mean that we have no comparable inelli, 2000). Indeed, there is also good evidence data on tactical deception in birds. One potential that chimpanzees perform better on physical tasks example is the cache-protection behavior of food- when they do not have to use a tool, compared to storing corvids. Strategies such as making false versions of the same task requiring tool use (Seed, caches (stones, small objects; Clayton, Griffi ths, & Call, et al., 2009). Th ere is also substantial evidence Bennett, 1996; Heinrich, 1999), as well as going that the physical cognition of non-tool-using ani- through the actions of caching but without deposit- mals is not fundamentally diff erent to that of tool- ing any items (Heinrich, 1999) could be classifi ed as using animals (Emery & Clayton, 2009b). examples of tactical deception as defi ned by Byrne Although there does not appear to be a striking and Whiten (1988). It has been suggested that cor- cognitive diff erence between tool users and nontool vids cache inedible objects in view of conspecifi cs, users, there are diff erences between species. Studies to learn about others’ pilfering intentions or pil- on corvids and apes have found a shared aptitude for fering techniques. To test this, Bugnyar and col- folk physics or understanding the functional prop- leagues (Bugnyar, Schwab, Schloegl, Kotrschal, & erties of tools. Using similar test paradigms, corvids Heinrich, 2007) allowed ravens to cache plastic and apes both demonstrate the ability to select, objects in front of either a pilfering (P) bird or an modify, and manufacture tools according to the spe- onlooker (O) human. After caching, P always stole cifi c demands of a given problem. New Caledonian the ravens’ caches, whereas O inspected the objects crows (NCC) and rooks spontaneously select tools but never stole them. Th e ravens were then allowed of a certain size or length to access concealed food to cache food; again in front of P or O. Ravens that items (crows, Chappell and Kacelnik, 2002, 2004; had experienced the P condition cached food more rooks, Bird and Emery, 2009a) as well as manufac- quickly, hid food behind obstructions, and made ture tools with respect to the functional require- more of an eff ort to conceal their stores than those ments of retrieval tasks (crows, Weir, Chappell, & in the O condition. However, this pattern was not Kacelnik, 2002; rooks, Bird and Emery, 2009a). repeated with objects, suggesting that the caching of Similarly, gorillas and orangutans are capable of inedible objects might be used as a deceptive tool to selecting tools with properties relevant to specifi c learn about an individual’s propensity to steal food tasks (Mulcahy, Call, & Dunbar, 2005). (Bugnyar et al., 2007). New Caledonian crows (Taylor, Hunt, Holzhaider, Another potential example of tactical deception & Gray, 2007; Taylor, Elliff e, Hunt, & Gray, 2010), is moving caches between cache sites in front of rooks (Bird & Emery, 2009a), gorillas, and orang-

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utans (Mulcahy et al., 2005) are also capable of Both species spontaneously solved the problem. In sequential tool use (i.e., using a small tool to acquire the case of the rooks, some water was contained a larger tool suitable for accessing food). Such tasks inside the tube, so the rooks dropped stones into are thought to present additional cognitive chal- the tube to raise the level of the water and thus lenges to that of regular tool use, because they require bring the food into reach. In the case of the orang- hierarchical forethought. Accordingly, the related utans, the tube contained no water, so the apes spat metatool use or use of one tool to shape another water into the tube, so that the food could fl oat to into a better tool (e.g., stone-knapping) represents within reach. an important breakthrough in hominid evolution Extractive foraging and tool-using behavior (St Amant & Horton, 2008). Although corvids and have thus been considered important mechanisms great apes rapidly accomplish sequential tool tasks, for driving the evolution of primate intelligence monkeys have had limited success, often persistently (Byrne, 1996, 2004; van Schaik, Deaner, & Merrill, attempting to retrieve a food reward directly with an 1999). Further support is also found in the relation- inadequate tool (Hihara, Obayashi, Tanaka, & Iriki, ship between relative brain size and the amount of 2003, Santos, Rosati, Sproul, Spaulding, & Hauser, reported tool use in primates (Reader & Laland, 2005). Corvids and apes, however, demonstrate an 2002) and birds (Lefebvre et al., 2002). However, advanced ability to manage their primary inhibi- the sophisticated understanding of the physical tions and organize their behaviors in a hierarchical properties of tools demonstrated by non-tool-us- fashion (Taylor et al., 2007). ing species, such as rooks (Bird & Emery, 2009a, Corvids and apes also demonstrate the ability 2009b), suggests the possibility of a domain-general to change the form of one object to manufacture a cognitive toolkit, rather than domain-specifi c adap- tool (such as break side twigs off a branch to make tive specializations that have evolved to solve spe- a straight stick) or shape and manipulate materials cifi c tool-related problems (Bird & Emery, 2009a, to make them into better tools (such as sculpting Emery & Clayton, 2009b). Such fi ndings question the end of a broken-off branch into a hook tool). previous accounts that correlate physical intelligence One apparent diff erence between corvids and apes specifi cally with tool use. is the ability of both NCC and rooks to manipu- late a seemingly nonfunctional (in the context of mental time travel the experiment) novel material (metal wire) into a Mental time travel (MTT) is the ability to recall new functional tool (a hook), which could then be subjective experiences and project oneself into the used to pull up a bucket containing food located past or future to re-experience or pre-experience in a vertical tube (Bird & Emery, 2009a; Weir et specifi c events. However, the unique component of al., 2002). Such behaviors suggest that these two such an episodic form of cognition, be it episodic species of corvids understood that, to retrieve the memory or future thinking, in contrast to seman- food, they had to (1) pull the bucket upward to tic knowledge, is that its utility invokes individual remove the food from the well, (2) recognize the perspectives that are detached from current mental inadequacies of the available tool (straight wire states (Clayton & Russell 2009; Raby & Clayton, instead of a hook), and (3) identify the malleable chapter 12 of this volume). properties of the wire (which could be fashioned Although MTT is a feature of human cogni- into a hook; Emery, 2006). What is perhaps most tion (Suddendorf & Corballis, 2008), recent work striking is that rooks do not use tools in the wild, has challenged the view that it is uniquely human so they must have formed a mental image of a suc- (Raby & Clayton, chapter 12 of this volume). To do cessful hook tool (which they had used in a previ- so, one must develop criteria that tap the behavioral ous study and which was completely diff erent in elements of episodic cognition, given that it is shape and structure to the available materials in impossible to test the phenomenological aspects the latter task) and modifi ed the novel material of re- and pre-experience in the absence of any into a hook based on this mental image. Rooks agreed behavioral markers of consciousness in non- (Bird & Emery, 2009b) and orangutans (Mendes, linguistic animals. Clayton and Dickinson (1998), Hanus, & Call, 2007) have also demonstrated therefore, suggested that one could test whether an innovative fl exibility when faced with a similar animal could remember the what, where, and when problem based on an Aesop’s fable in which food of a specifi c event, and termed this “episodic-like” was located inside a vertical tube without a bucket. memory. Hence descriptions of MTT in nonverbal

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animals are often referred to as episodic-like or what- to the room where breakfast was provided. In a where-when (WWW) memory. second “breakfast-choice” experiment, Raby and A number of studies have subsequently shown that colleagues (2007) controlled for any conditioning this form of MTT, or WWW memory, is present in that may have infl uenced caching in places associ- a variety of nonhuman animals, including corvids ated with hunger by always providing breakfast in (Clayton & Dickinson, 1998; Zinkivskay, Nazir, & each room. However, in this experiment, each room Smulders, 2009), chickadees (Feeney, Roberts, & was associated with a particular type of food (i.e., Sherry, 2009), apes (Martin-Ordas, Haun, & Call, dog kibble or peanuts). If the jays based their cach- 2010) and rats (Babb & Crystal, 2006a, 2006b). ing decisions on a conditioned response, formed Subsequently, it has also been found that animals from associating a particular room with a particular can take action now for the future, suggesting that food, they would be predicted to cache dog kibble they also have the prospective component of MTT in the room previously associated with dog kibble (for example, Correia, Dickinson, & Clayton, 2007; and vice versa. However, jays in this experiment Mulcahy & Call, 2006; Osvath, 2009; Osvath & cached more of the diff erent food rather than the Osvath, 2008; Raby, Alexis, Dickinson, & Clayton, same food in each room, suggesting that they pre- 2007). ferred a choice of food at breakfast and were capable Possibly the most convincing evidence for MTT of forward planning (Raby et al., 2007). in nonhuman animals has been documented for cor- Using a similar methodology to Clayton and vids and apes. Capitalizing on their natural propen- Dickinson (1998), but with preferred perishable sity to cache food, detailed experiments on Western (because it was frozen and could melt) juice and less scrub jays have revealed that they understand what preferred, but nonperishable grapes, Martin-Ordas items of food they stored, where they stored them, and colleagues (2010) recently found that chim- and when these items were stored (Clayton & panzees, orangutans and bonobos were capable of Dickinson, 1998). Clayton and Dickinson (1998) distinguishing between diff erent events in which presented jays with the opportunity to cache per- the same food items were hidden in diff erent places ishable wax worms and nonperishable peanuts. at diff erent times, suggesting that the apes also Following caching, the jays were subjected to two remembered in an integrated fashion what, where experimental conditions of either a short delay prior and when certain events occurred (Martin-Ordas to retrieval (4 hrs) or a long delay (124 hrs). After et al., 2010). a short delay, jays preferentially searched for wax Likewise, Mulcahy and Call (2006), found that worms, which were favored over peanuts. However, apes are capable of selecting, transporting, and after experiencing a long delay, in which the worms saving a suitable tool, not because they currently had decayed and become inedible, jays avoided needed it, but because they would need it in the searching for the worms and instead recovered pea- future. Apes learned to use a tool to obtain a reward nuts. Th e preferential recovery of particular food from an apparatus. In a separate testing room with items, depending on when they were cached, sug- no apparatus, the apes were then provided with a gests that the jays used an episodic-like memory to choice of one out of two suitable and six unsuit- recall past experiences about the degradation rates able tools. Th e subjects then experienced either a 1- of diff erent food types, as well as where and when or 14-hour delay after which they were allowed to each item of food was stored. return to the test room, with their selected tool, to Further experiments have revealed that jays’ access the apparatus. Th e apes succeeded in select- caching decisions are constructed from anticipat- ing and retaining appropriate tools for future use ing their future needs, irrespective of their current (Mulcahy & Call, 2006). Similar results were also motivational states (Correia et al., 2007; Raby et al., found in studies that increased the cognitive load of 2007). Raby and colleagues (2007) housed jays subjects by disassociating the locations of the tool in one of two separate rooms over six alternative and apparatus as well as increasing the delay period days. In one room, they were always given breakfast and housing subjects socially instead of individually and in the other they were not. After this training (Osvath & Osvath, 2008). period, the jays were unexpectedly given food to eat and cache in the evening. Raby and colleagues Welcome to the Clever Club (2007) found that the jays stored more food in Although we have primarily restricted our arguments the nonbreakfast room, where they could expect to corvids and apes, we have included examples from to be hungry the following morning, compared other animals where appropriate. Indeed, there is

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CORVIDS PARROTS APES CETACEANS ELEPHANTS Diet Omnivorous Omnivorous Omnivorous Carnivorous Herbivorous

Tool Use

Social System

Brain

Crocodilians Dinosaurs

Turtles Diapsids Anapsids Therapsids

Stem Amniote

Figure 5.3 Upper. Diagram displaying various biological (brain structure), ecological (diet), and behavioral (tool use [stick use by New Caledonian crows, wood- tool aid to opening palm nuts in hyacinth macaws, termite fi shing in chimpanzees, sponge-tool use by dolphins, fl y switching by elephants]), and social-system (black and white fi gures represent diff erent individuals within a social group and so the variety of individuals suggest social complexity) traits in corvids, parrots, apes, cetaceans, and elephants. Despite very diff erent brain structures, such as the lack of cortical folding in birds but extensive folding in apes, cetaceans, and elephants, there are striking similarities in the diet, use of tools, and social system, in these distantly related animal groups. Lower. Basic evolutionary tree displaying the relationships between these main animal groups.

good evidence that cetaceans (whales and dolphins) corvids and apes because they have solved similar also demonstrate convergent evolution of cognition environmental problems, then we should expect with apes (Marino, 2002). We could extend the invi- groups that have faced similar problems to have tation to parrots; possibly other groups of birds with evolved similar solutions to these problems. Th is relatively large brains, behavioral fl exibility, and a could be in the form of complex behavioral strategies complex diet, such as hornbills and some birds of or cognitive processes. Based on a simple analysis of prey; elephants; and pack-hunting carnivores, such such problems and similar life-history traits, Emery as hyenas (see Emery, 2006). We would not extend (2006) found that many animal groups displayed the invitation to domestic dogs because their cogni- similar traits at the biological, ecological, behavioral tive abilities, impressive as they are (Miklosi, 2007) and psychological levels (Figure 5.3). Underlying cannot be an example of convergence, because their all of these similarities is behavioral fl exibility as cognitive evolution is likely the result of domesti- applied to the solution of problems faced by living cation by humans, rather than a response to socio- in an unpredictable environment (Sterleny, 2003). ecological selection pressures in their adaptive As such, those species with a varied, ephemeral, and environment. Domestication thus seems to be the even unpredictable diet, that lived in a complex (but most appropriate hypothesis to explain dogs’ intelli- not necessarily large) society, that had a relatively gence, especially in the social realm (but see Miklosi large brain, went through a long developmental & Topal, chapter 11 of this volume). period, lived a long life, and lived in a fl uctuating If our hypothesis is correct, that shared cognitive habitat, could all be considered candidates for con- traits have arisen in distantly related groups such as vergent evolution.

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Conclusion Barton, R. A. (1996). Neocortex size and behavioural ecology in It is likely that there is no one particular mechanism primates. Proceedings of the Royal Society B, 263, 173–177. Barton, R. A. (1998).Visual specialization and brain evolu- that is responsible for driving the evolution of cog- tion in primates. Proceedings of the Royal Society B, 265, nition across all species. Cognition is, instead, likely 1933–1937. to have evolved as a result of the many challenges Beck, B. B. (1980). Animal tool behaviour. New York: Garland. animals face in their environments. Group living Bednekoff , P. A., & Balda, R. P. (1996a). Observational spatial may have provided a foundation for social cogni- memory in Clark’s nutcrackers and Mexican jays. Animal Behaviour, 52, 833–839. tion and, hence, social cooperation and manipu- Bednekoff , P. A., & Balda, R. P. (1996b). Social caching and lation, but qualitative relationships in the form of observational spatial memory in pinyon jays. Behaviour, 133, monogamous pair bonds or the arms race between 807–826. cachers and pilferers may have also been important. Beggs, J. R., & Wilson, P. R. (1987). Energetics of South Similarly, methods for manipulating the environ- Island kaka (Nestor meridionalis meridionalis) feeding on the larvae of kanuka longhorn beetles (Ochrocydus huttoni). ment, such as building a nest or extractive foraging New Zealand Journal of Ecology, 10, 143–147. (with or without tool use) may have provided the Benham, W. B. (1906). Notes on the fl esh-eating propensity of foundation for physical cognition. Although still the kea (Nestor notabilis). Transactions of the Royal Society of not clear, it seems probable that neither the social New Zealand, 39, 71–89. or physical realm alone drove the evolution of intel- Bennett, P. M., & Harvey, P. H. (1985). Brain size, development and metabolism in birds and mammals. Journal of Zoology, ligence. Rather, the ability to adapt to a changing 207, 491–509. environment, as encountered by the species under Bird, C. D., & Emery, N. J. (2009a). Insightful problem solv- consideration here, is perhaps the best explanation ing and creative tool modifi cation by captive nontool-using we have for why some animals display the cognitive rooks. PNAS, 106, 10370–10375. abilities they do and why such abilities have evolved Bird, C. D., & Emery, N. J. (2009b). Rooks use stones to raise the water level to reach a fl oating worm. Current Biology, 19, convergently in very distantly related groups. 1410–1414. Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Future Directions Sousa, C., & Matsuzawa, T. (2003). Cultural innovation and 1. Are the behavioral similarities of corvids transmission of tool use in wild chimpanzees: Evidence from and apes (and other animals) based on a fi eld experiments. Animal Cognition, 6, 213–223. similar cognitive architecture? How can this be Bitterman, M. E. (1960). Toward a comparative psychology of learning. American Psychologist, 15, 704–712. investigated empirically? Bitterman, M. E. (1965). Phyletic diff erences in learning. 2. What features of the social and physical American Psychologist, 20, 396–410. environment may have driven cognitive Boesch, C., & Boesch, H. (1990). Tool use and tool making in convergence in corvids, apes, and other animal wild chimpanzees. Folia Primatologica, 54, 86–99. groups, such as parrots, cetaceans, and elephants? Bolhuis, J. J., & Macphail, E. M. (2001). A critique of the neuroecology of learning and memory. Trends in Cognitive 3. How do convergences in cognition occur Sciences, 5, 426–433. with divergences in neural structures? Borsari, A.,& Ottoni, E. B. (2005). Preliminary observations of tool use in captive hyacinth macaws (Anodorhynchus hyacin- References thinus). Animal Cognition, 8, 48–52. Aiello, L. C., & Wheeler, P. (1995). Th e expensive-tissue hypothesis: Brauer, J., Call, J., & Tomasello, M. (2005). All great ape species Th e brain and the digestive system in human and primate follow gaze to distant locations and around barriers. Journal evolution. Current Anthropology, 36, 199–221. of Comparative Psychology, 119, 145–154. Aureli, F., Schaff ner, C. M., Boesch, C., Bearder, S. K., Call, J., Bugnyar, T., & Heinrich, B. (2005). Ravens, Corvus corax, dif- Chapman, C. A., Connor, R., Di Fiore, A., Dunbar, R. I. M., ferentiate between knowledgeable and ignorant competitors. Henzi, S. P., Holekamp, K., Korstjens, A. H., Layton, R., Proceedings of the Royal Society B, 272, 1641–1646. Lee, P., Lehmann, J., Manson, J. H., Ramos-Fernandez, G., Bugnyar, T., & Kotrschal, K. (2002). Observational learning and Strier, K. B., & van Schaik, C. P. (2008). Fission-Fusion the raiding of food caches in ravens (Corvus corax): Is it ‘tacti- Dynamics New Research Frameworks. Current Anthropology, cal’ deception? Animal Behaviour, 64, 185–195. 49, 627–654. Bugnyar, T., Schwab, C., Schloegl, C., Kotrschal, K., & Heinrich, Babb, S. J., & Crystal, J. D. (2006a). Discrimination of what, B. (2007). Ravens judge competitors through experience when, and where is not based on time of day. Learning & with play caching. Current Biology, 17, 1804–1808. Behavior, 34, 124–130. Bugnyar, T., Stowe, M., & Heinrich, B. (2004). Ravens, Corvus corax, Babb, S. J., & Crystal, J. D. (2006b). Episodic-like memory in follow gaze direction of humans around obstacles. Proceedings of the rat. Current Biology, 16, 1317–1321. the Royal Society of London Series B, 271, 1331–1336. Balda, R. P., & Kamil, A. C. (1992). Long-term spatial mem- Burish, M. J., Kueh, H. Y., & Wang, S. S. H. (2004). Brain ory in Clark nutcracker (Nucifraga columbiana). Animal architecture and social complexity in modern and ancient Behaviour, 44, 761–769. birds. Brain Behavior & Evolution, 63, 107–124.

96 convergent evolution of cognition in corvids, apes and other animals

005_Vonk_Ch05.indd5_Vonk_Ch05.indd 9966 110/18/20110/18/2011 88:15:12:15:12 PPMM OUP UNCORRECTED PROOF – FIRST-PROOF, 10/18/11, NEWGEN

Byrne, R. W. (1996). Th e misunderstood ape: Cognitive skills mammals. Philosophical Transactions of the Royal Society B, of the gorilla. In A. E. Russon, K. A. Bard, & S. T. Parker 362, 587–602. (Eds.) Reaching into Th ought: Th e Minds of the Great Apes. Connor, R. C., Mann, J., Tyack, P. L., & Whitehead, H. (1998). Cambridge, UK: Cambridge University Press. Social evolution in toothed whales. Trends in Ecology & Byrne, R. W. (2004). Th e manual skills and cognition that lie Evolution, 13, 228–232. behind hominid tool use. In A. E. Russon, & D. R. Begun Connor, R. C., Smolker, R. A., & Richards, A. F. (1992). (Eds.) Th e Evolution of Th ought: Evolutionary Origins of Great Dolphin alliances and coalitions. In A. H. Harcourt, & Ape Intelligence. Cambridge, UK,: Cambridge University Press. F. B. M. de Waal (Eds.) Coalitions and Alliances in Humans Byrne, R. W., & Bates, L. A. (2009). Elephant cognition in pri- and Other Animals, pp. 415–443. Oxford, UK: Oxford mate perspective. Comparative Cognition & Behavior Reviews, University Press. 4, 65–79. Correia, S. P. C., Dickinson, A., & Clayton, N. S. (2007). Western Byrne, R. W., & Corp, N. (2004). Neocortex size predicts decep- scrub-jays anticipate future needs independently of their cur- tion rate in primates. Proceedings of the Royal Society B, 271, rent motivational state. Current Biology, 17, 856–861. 1693–1699. Cramp, S., & Perrins, C. (1994). Th e birds of the Western Byrne, R. W., & Whiten, A. (1985). Tactical deception of famil- Palearctic. Crows to fi nches. In Handbook of the Birds of iar individuals in baboons (Papio ursinus). Animal Behaviour, Europe, the Middle East and North Africa. Oxford, UK: 33, 669–673. Oxford University Press. Byrne, R. W., & Whiten, A. (1988). Machiavellian Intelligence: Cristol, D. A., & Switzer, P. V. (1999). Avian prey-dropping Social expertise and the evolution of intellect in monkeys, apes, behavior. II. American crows and walnuts. Behavioral Ecology, and humans. Oxford, UK: Clarendon Press. 10, 220–226. Call, J., Agnetta, B., & Tomasello, M. (2000). Social cues that Cuthbert, R. (2003). Sign left by introduced and native preda- chimpanzees do and do not use to fi nd hidden objects. tors feeding on Hutton’s shearwaters (Puffi nus huttoni). New Animal Cognition, 3, 23–34. Zealand Journal of Zoology, 30, 163–170. Call, J., Hare, B., & Tomasello, M. (1998). Chimpanzee gaze Dally, J. M., Clayton, N. S., & Emery, N. J. (2006a). Th e behav- following in an object-choice task. Animal Cognition, 1, iour and evolution of cache protection and pilferage. Animal 89–99. Behaviour, 72, 13–23. Chappell, J., & Kacelnik, A. (2002). Tool selectivity in a non- Dally, J. M., Emery, N. J., & Clayton, N. S. (2004). Cache primate, the New Caledonian crow (Corvus moneduloides). protection strategies by Western scrub-jays (Aphelocoma Animal Cognition, 5, 71–78. californica): hiding food in the shade. Proceedings of the Royal Chappell, J., & Kacelnik, A. (2004). Selection of tool diameter Society B, 271 Suppl 6, S387–390. by New Caledonian crows (Corvus moneduloides). Animal Dally, J. M., Emery, N. J., & Clayton, N. S. (2005). Cache pro- Cognition, 7, 121–127. tection strategies by Western scrub-jays (Aphelocoma califor- Clark, C. M. H. (1970). Observations on population, move- nica): implications for social cognition. Animal Behaviour, ments and food of the kea (Nestor notabilis). Notornis, 17, 70, 1251–1263. 105–114. Dally, J. M., Emery, N. J., & Clayton, N. S. (2006b). Food- Clayton, N. S., Dally, J. M., & Emery, N. J. (2007). Social cog- caching Western scrub-jays keep track of who was watching nition by food-caching corvids: Th e Western scrub-jay as a when. Science, 312, 1662–1665. natural psychologist. Philosophical Transactions of the Royal Deaner, R. O., Isler, K., Burkart, J., & van Schaik, C. P. (2007) Society B, 362, 507–522. .Overall brain size, and not encephalization quotient, best Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory predicts cognitive ability across non-human primates. Brain during cache recovery by scrub jays. Nature, 395, 272–274. Behavior & Evolution, 70, 115–124. Clayton, N. S., & Dickinson, A. (1999). Scrub jays (Aphelocoma de Kort, S. R., Dickinson, A., & Clayton, N. S. (2005). coerulescens) remember the relative time of caching as well Retrospective cognition by food-caching western scrub-jays. as the location and content of their caches. Journal of Learning and Motivation, 36, 159–176. Comparative Psychology, 113, 403–416. de Kort, S. R., Emery, N. J., & Clayton, N. S. (2003). Food Clayton, N. S., Griffi ths, D. P., & Bennett, A. D. (1996). Storage off ering in jackdaws (Corvus monedula). Naturwissenschaften, of stones by jays (Garrulus glandarious). Ibis, 136, 331–334. 90, 238–240. Clayton, N. S., & Russell, J. (2009). Looking for episodic cog- de Waal, F. B. M. (1982). Chimpanzee politics, London: Jonathan nition in animals and young children: prospects for a new Cape. minimalism. Neuropsychologica, 47, 2330–2340. de Waal, F. B. M., & Lutrell, L. M. (1988). Mechanisms of social Clayton, N. S., Yu, K. S., & Dickinson, A. (2001). Scrub jays reciprocity in three primate species: symmetrical relation- (Aphelocoma coerulescens) form integrated memories of the ship characteristics or cognition? Ethology and Sociobiology, multiple features of caching episodes. Journal of Experimental 101–118. Psychology-Animal Behavior Processes, 27, 17–29. de Waal, F. B. M., & Tyack, P. L. (2003). Animal social complex- Clayton, N. S., Yu, K. S., & Dickinson, A. (2003). Interacting ity. Cambridge, MA: Harvard University Press. cache memories: Evidence for fl exible memory use by Western Diamond, J., & Bond, A. B. (1999). Kea, Bird of Paradox: Th e scrub-Jays (Aphelocoma californica). Journal of Experimental evolution and behaviour of a New Zealand parrot. Berkley, Psychology-Animal Behavior Processes, 29, 14–22. CA: University of California Press. Clutton-Brock, T. H., & Harvey, P. H. (1980). Primates, brains Dunbar, R. I. M. (1992). Neocortex size as a constraint on group- and ecology. Journal of Zoology, 190, 309–323. size in primates. Journal of Human Evolution, 22, 469–493. Connor, R. C. (2007). Dolphin social intelligence: complex alli- Dunbar, R. I. M. (1995). Neocortex size and group-size in pri- ance relationships in bottlenose dolphins and a consideration mates—A test of the hypothesis. Journal of Human Evolution, of selective environments for extreme brain size evolution in 28, 287–296.

van horik, clayton, emery 97

005_Vonk_Ch05.indd5_Vonk_Ch05.indd 9977 110/18/20110/18/2011 88:15:12:15:12 PPMM OUP UNCORRECTED PROOF – FIRST-PROOF, 10/18/11, NEWGEN

Dunbar, R. I. M. (1998). Th e social brain hypothesis. Evolutionary Gibson, K. R. (1986). Cognition, brain size and the extrac- Anthropology, 6, 178–190. tion of embedded food resources. In J. G. Else, & P. C. Lee Emery, N. J. (2000). Th e eyes have it: Th e neuroethology, (Eds.) Primate Ontogeny, Cognition and Social Behaviour. function and evolution of social gaze. Neuroscience and pp. 93–105. Cambridge, UK: Cambridge University Press. Biobehavioral Reviews, 24, 581–604. Giret, N., Miklosi, A., Kreutzer, M., & Bovet, D. (2009). Use Emery, N. J. (2004). Are corvids “feathered apes”? Cognitive of experimenter-given cues by African gray parrots (Psittacus evolution in crows, jays rooks and jackdaws. In: Watanabe, S. erithacus). Animal Cognition, 12, 1–10. (Ed.) Comparative Analysis of Minds. pp. 181–213. Tokyo, Goodall, J. (1963). Feeding behaviour of wild chimpanzees: a Japan, Keio University Press. preliminary report. Symposium of the Zoological Society of Emery, N. J. (2006). Cognitive ornithology: Th e evolution of London, 10, 39–48. avian intelligence. Philosophical Transactions of the Royal Goodall, J. (1986). Th e chimpanzees of Gombe: Patterns of behav- Society B, 361, 23–43. ior. Cambridge, MA: Harvard University Press. Emery, N. J., & Clayton, N. S. (2001). Eff ects of experience and Hain, J. H. W., Carter, G. R., Kraus, S. D., Mayo, C. A., & social context on prospective caching strategies by scrub jays. Winn, H. E. (1982). Feeding behavior of the humpback Nature, 414, 443–446. whale, Megaptera novaeangliae, in the Western North- Emery, N. J., & Clayton, N. S. (2004a). Comparing the complex Atlantic. Fishery Bulletin, 80, 259–268. cognition of birds and primates In L. J. Rogers & G. Kaplan Hare, B., Brown, M., Williamson, C., & Tomasello, M. (2002). (Eds.) Comparative Vertebrate Cognition: Are primates superior Th e domestication of social cognition in dogs. Science, 298, to nonprimates? pp. 3–55. New York: Kluwer. 1634–1636. Emery, N. J., & Clayton, N. S. (2004b). Th e mentality of crows: Hare, B., Call, J., Agnetta, B., & Tomasello, M. (2000). convergent evolution of intelligence in corvids and apes. Chimpanzees know what conspecifi cs do and do not see. Science, 306, 1903–1907. Animal Behaviour, 59, 771–785. Emery, N. J., & Clayton, N. S. (2008). How to build a scrub-jay Hare, B., Call, J., & Tomasello, M. (2001). Do chimpan- that reads minds. In S. Itakura & K. Fujita (Eds.) Origins zees know what conspecifi cs know? Animal Behaviour, 61, of the Social Mind: Evolutionary & developmental views. 139–151. pp. 65–97 . Tokyo: Springer Japan. Hare, B., & Tomasello, M. (2005) Human-like social skills in Emery, N. J., & Clayton, N. S. (2009a). Comparative social cog- dogs? Trends in Cognitive Sciences, 9, 439–444. nition. Annual Review of Psychology, 60, 87–113. Healy, S. D., & Rowe, C. (2007). A critique of comparative Emery, N. J., & Clayton, N. S. (2009b). Tool use and physi- studies of brain size. Proceedings of the Royal Society B, 274, cal cognition in birds and mammals. Current Opinion in 453–464. Neurobiology, 19, 27–33. Heinrich, B. (1999) Mind of the Raven, New York, Harper Emery, N. J., Clayton, N. S., & Frith, C. D. (2007a). Introduction. Collins Publishers. Social intelligence: from brain to culture. Philosophical Herrmann, E., Hare, B., Call, J., & Tomasello, M. (2010) Transactions of the Royal Society B, 362, 485–488. .Diff erences in the cognitive skills of bonobos and chimpan- Emery, N. J., Lorincz, E. N., Perrett, D. I., Oram, M. W., & zees. PLoS One, 5, e12438. Baker, C. I. (1997). Gaze following and joint attention in Hihara, S., Obayashi, S., Tanaka, M., & Iriki, A. (2003). rhesus monkeys (Macaca mulatta). Journal of Comparative Rapid learning of sequential tool use by macaque monkeys. Psychology, 111, 286–293. Physiology & Behavior, 78, 427–434. Emery, N. J., Seed, A. M., von Bayern, A. M. P., & Clayton, Hodos, W. (1993). Th e Visual Capabilities of Birds. In H. P. N. S. (2007b). Cognitive adaptations of social bonding in Zeigler & H. J. Bischof (Eds.) Vision, brain, and behavior in birds. Philosophical Transactions of the Royal Society B, 362, birds. Cambridge, MA: MIT Press. 489–505. Hohmann, G., & Fruth, B. (2008). New records on prey capture Engh, A. L., Siebert, E. R., Greenberg, D. A., & Holekamp, K. and meat eating by bonobos at Lui Kotale, Salonga National E. (2005). Patterns of alliance formation and postconfl ict Park, Democratic Republic of Congo. Folia Primatologica, aggression indicate spotted hyaenas recognize third-party 79, 103–110. relationships. Animal Behaviour, 69, 209–217. Holekamp, K. E., Sakai, S. T., & Lundrigan, B. L. (2007). Feeney, M. C., Roberts, W. A., & Sherry, D. F. (2009). Memory Social intelligence in the spotted hyena (Crocuta cro- for what, where, and when in the black-capped chickadee cuta). Philosophical Transactions of the Royal Society B, 362, (Poecile atricapillus). Animal Cognition, 12, 767–777. 523–538. Fragasky, D., Izar, P., Visalberghi, E., Ottoni, E. B., & de Huber, L., & Gajdon, G. K. (2006) .Technical intelligence in Oliveira, M. G. (2004). Wild capuchin monkeys (Cebus animals: the kea model. Animal Cognition, 9, 295–305. libidinosus) use anvils and stone pounding tools. American Humphrey, N. K. (1976). Th e social function of intellect In P. P. Journal of Primatology, 64, 359–366. G. Bateson, & R. A. Hinde (Eds.) Growing Points in Ethology. Fragaszy, D., Pickering, T., Liu, Q., Izar, P., Ottoni, E., & pp. 303–317. Cambridge, MA: Cambridge University Press. Visalberghi, E. (2010). Bearded capuchin monkeys’ and a Hunt, G. R. (1996). Manufacture and use of hook-tools by New human’s effi ciency at cracking palm nuts with stone tools: Caledonian crows. Nature, 379, 249–251. Field experiments. Animal Behaviour, 79, 321–332. Hunt, G. R., Corballis, M. C., & Gray, R. D. (2006). Design Gajdon, G. K., Fijn, N., & Huber, L. (2006). Limited spread of complexity and strength of laterality are correlated in New innovation in a wild parrot, the kea (Nestor notabilis). Animal Caledonian crows’ Pandanus tool manufacture. Proceedings of Cognition, 9, 173–181. the Royal Society B, 273, 1127–1133. Garamszegi, L. Z., Moller, A. P., & Erritzoe, J. (2002). Coevolving Hunt, G. R., & Gray, R. D. (2004). Th e crafting of hook tools by avian eye size and brain size in relation to prey capture and noc- wild New Caledonian crows. Proceedings of the Royal Society turnality. Proceedings of the Royal Society B, 269, 961–967. B: Biology Letters, 271 (S3), S88–S90.

98 convergent evolution of cognition in corvids, apes and other animals

005_Vonk_Ch05.indd5_Vonk_Ch05.indd 9988 110/18/20110/18/2011 88:15:13:15:13 PPMM OUP UNCORRECTED PROOF – FIRST-PROOF, 10/18/11, NEWGEN

Husband, S., & Shimizu, T. (2001). Evolution of the avian visual Marino, L., Connor, R. C., Fordyce, R. E., Herman, L. M., Hof, system. In R. G. Cook (Ed.) Avian Visual Cognition. Available P. R., Lefebvre, L., Lusseau, D., McCowan, B., Nimchinsky, on-line: www.pigeon.psy.tufts.edu/avc/shimp. E. A., Pack, A. A., Rendell, L., Reidenberg, J. S., Reiss, D., Isler, K., & van Schaik, C. P. (2009). Why are there so few Uhen, M. D., van der Gucht, E., & Whitehead, H. (2007). smart mammals (but so many smart birds)? Biology Letters, Cetaceans have complex brains for complex cognition. PLoS 5, 125–129. Biology, 5, 966–972. Iwaniuk, A. N., & Nelson, J. E. (2003). Developmental dif- Martin-Ordas, G., Haun, D., Colmenares, F., & Call, J. (2010). ferences are correlated with relative brain size in birds: a Keeping track of time: evidence for episodic-like memory in comparative analysis. Canadian Journal of Zoology, 81, great apes. Animal Cognition, 13, 331–340. 1913–1928. Mendes, N., Hanus, D., & Call, J. (2007). Raising the level: Janmaat, K. R. L., Byrne, R. W., & Zuberbuhler, K. (2006). orangutans use water as a tool. Biology Letters, 3, 453–455. Evidence for a spatial memory of fruiting states of rainforest Miklosi, A. (2007). Dogs: Behavior, evolution & cognition, trees in wild mangabeys. Animal Behaviour, 72, 797–807. New York: Oxford University Press. Jerison, H. J. (1973). Evolution of the Brain and Intelligence, Miklosi, A., Topal, J., & Csanyi, V. (2004). Comparative social New York, Academic Press. cognition: what can dogs teach us? Animal Behaviour, 67, Jolly, A. (1966). Lemur social behavior and primate intelligence. 995–1004. Science, 153, 501–506. Miklosi, A., & Soproni, K. (2006) A comparative analysis of ani- Jones, T. B., & Kamil, A. C. (1973) Tool-making and tool-using mals’ understanding of the human pointing gesture. Animal in the northern blue jay. Science, 180, 1076–1078. Cognition, 9, 81–93. Juniper, T., & Parr, M. (2003). Parrots: A guide to the parrots of Milton, K. (1981). Distribution patterns of tropical plant foods the world. as an evolutionary stimulus to primate mental-development. Jurasz, C. M., & Jurasz, V. P. (1979) Feeding modes of the American Anthropologist, 83, 534–548. humpback whale Megaptera novaeangliae in Southeastern Moorhouse, R. J. (1997). Th e diet of the North Island kaka Alaska USA. Scientifi c Reports of the Whales Research Institute (Nestor meridionalis septentrionalis) on Kapiti Island. New Tokyo, 69–84. Zealand Journal of Ecology, 21, 141–152. Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2005). Mulcahy, N. J., & Call, J. (2006). Apes save tools for future use. Domestic goats, Capra hircus, follow gaze direction and use Science, 312, 1038–1040. social cues in an object choice task. Animal Behaviour, 69, Mulcahy, N. J., Call, J., & Dunbar, R. I. M. (2005). Gorillas 11–18. (Gorilla gorilla) and Orangutans (Pongo pygmaeus) encode Karin-D’Arcy, M. R., & Povinelli, D. J. (2002). Do chimpan- relevant problem features in a tool-using task. Journal of zees know what each other see? A closer look. International Comparative Psychology, 119, 23–32. Journal of Comparative Psychology, 15, 21–54. Nicolson, N. A. (1986). Infants, mothers, and other females. Keeton, W. T., & Gould, J. L. (1986). Biological science. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. New York: Norton. Wrangham, & T. T. Struhsaker (Eds.) Primate societies. Leatherwood, S. (1975). Some observations of feeding behavior Chicago: University of Chicago Press. of bottle-nosed dolphins (Tursiops truncatus) in Northern Nikei, Y. (1995). Variations of behaviour of carrion crows (Corvus Gulf-of-Mexico and (Tursiops cf Tursiops gilli) off Southern- corone) using automobiles as nutcrackers. Japanese Journal of California, Baja-California, and Nayarit, Mexico. Marine Ornithology, 44, 21–35. Fisheries Review, 37, 10–16. Osvath, M. (2009). Spontaneous planning for future stone throw- Lefebvre, L., Nicolakakis, N., & Boire, D. (2002). Tools and ing by a male chimpanzee. Current Biology, 19, R190–R191. brains in birds. Behaviour, 139, 939–973. Osvath, M., & Osvath, H. (2008). Chimpanzee (Pan troglo- Lefebvre, L., Reader, S. M., & Sol, D. (2004). Brains, innova- dytes) and orangutan (Pongo abelii) forethought: Self-control tions and evolution in birds and primates. Brain Behavior & and pre-experience in the face of future tool use. Animal Evolution, 63, 233–246. Cognition, 11, 661–674. Lefebvre, L., Whittle, P., Lascaris, E., & Finkelstein, A. (1997). Papini, M. R. (2002). Pattern and process in the evolution of Feeding innovations and forebrain size in birds. Animal learning. Psychological Review, 109, 186–201. Behaviour, 53, 549–560. Parker, S. T., & Gibson, K. R. (1977). Object manipulation, tool Liedtke, J., Werdenich, D., Gajdon, G. K., Huber, L., & Wanker, R. use and sensorimotor intelligence as feeding adaptations in (2010). Big brains are not enough: Performance of three par- cebus monkeys and great apes. Journal of Human Evolution, rot species in the trap-tube paradigm. Animal Cognition, 14, 6, 623–641. 143–149. Pepperberg, I. M. (1999). Th e Alex studies: Cognitive and com- Lockie, J. D. (1955). Th e breeding and feeding of jackdaws and municative abilities of grey parrots, Cambridge, MA: Harvard rooks with notes on carrion crows and other corvidae. Ibis, University Press. 97, 341–368. Potts, R. (2004). Paleoenvironmental basis of cognitive evolution Lonsdorf, E. V. (2006). What is the role of mothers in the in great apes. American Journal of Primatology, 62, 209–228. acquisition of termite-fi shing behaviors in wild chimpan- Povinelli, D. J. (2000). Folk Physics for Apes. New York: Oxford zees (Pan troglodytes schweinfurthii)? Animal Cognition, 9, University Press. 36–46. Povinelli, D. J., & Vonk, J. (2004). We don’t need a microscope Marino, L. (1996). What can dolphins tell us about primate evo- to explore the chimpanzees’ mind. Mind & Language, 19, lution? Evolutionary Anthropology, 5, 81–86. 1–28. Marino, L. (2002). Convergence of complex cognitive abilities Raby, C. R., Alexis, D. M., Dickinson, A., & Clayton, N. S. in cetaceans and primates. Brain Behavior & Evolution, 59, (2007). Planning for the future by western scrub-jays. 21–32. Nature, 445, 919–921.

van horik, clayton, emery 99

005_Vonk_Ch05.indd5_Vonk_Ch05.indd 9999 110/18/20110/18/2011 88:15:13:15:13 PPMM OUP UNCORRECTED PROOF – FIRST-PROOF, 10/18/11, NEWGEN

Range, F., & Noe, R. (2005). Can simple rules account for the St Amant, R., & Horton, T. E. (2008). Revisiting the defi nition pattern of triadic interactions in juvenile and adult female of animal tool use. Animal Behaviour, 75, 1199–1208. sooty mangabeys? Animal Behaviour, 69, 445–452. Starck, J. M. (1993) Evolution of avian ontogenies. In D. M. Reader, S. M., & Laland, K. N. (2002). Social intelligence, Power (Ed.) Current Ornithology. New York: Plenum Press. innovation, and enhanced brain size in primates. PNAS, 99, Starck, J. M., & Riclefs, R. E. (1998). Patterns of development: 4436–4441. the altricial–precocial spectrum. In J. M. Starck, & R. E. Reiner, A., Perkel, D. J., Bruce, L. L., Butler, A. B., Csillag, A., Ricklefs (Eds.) Avian growth and development: Evolution Kuenzel, W., Median, L., Paxinos, G., Shimizu, T., Striedter, within the altricial–precocial spectrum. Oxford, UK: Oxford G., Wild, M., Ball, G. F., Durand, S., Gunturkun, O., Lee, University Press. D. W., Mello, C. V., Powers, A., White, S. A., Hough, G., Sterelny, K. (2003). Th ought in a Hostile World, Oxford, Kubikova, L., Smulders, T. V., Wada, K., Dugas-Ford, J., Blackwell. Husband, S., Yamamoto, K., Yu, J., Siang, C., & Jarvis, E. Striedter, G. F. (2005). Principles of Brain Evolution, Sunderland, D. (2004). Revised nomenclature for avian telencephalon MA: Sinauer Associates. and some related brainstem nuclei. Journal of Comparative Suddendorf, T., & Corballis, M. C. (2008). New evidence for Neurology, 473, 377–414. animal foresight? Animal Behaviour, 75, E1–E3. Rehkamper, G., Frahm, H. D., & Zilles, K. (1991). Taylor, A. H., Elliff e, D., Hunt, G. R., & Gray, R. D. (2010). Quantitative development of brain and brain structures in Complex cognition and behavioural innovation in New birds (Galliformes and Passeriformes) compared to that in Caledonian crows. Proceedings of the Royal Society B, 277, mammals (insectovores and primates). Brain Behavior and 2637–2643. Evolution, 37, 125–143. Taylor, A. H., Hunt, G. R., Holzhaider, J. C., & Gray, R. D. Ricklefs, R. E. (2004). Th e cognitive face of avian life histories. (2007). Spontaneous metatool use by new Caledonian crows. Wilson Bulletin, 116, 119–133. Current Biology, 17, 1504–1507. Ridley, M. (1993). Evolution. Oxford, UK: Blackwell. Tebbich, S., Taborsky, M., Fessl, B., & Dvorak, M. (2002). Th e Ross, C. (2004). Life histories and the evolution of large brain ecology of tool use in the woodpecker fi nch (Cactospiza pal- size in great apes. In A. E. Russon, & D. R. Begun (Eds.) Th e lida). Ecology Letters, 5, 656–664. Evolution of Th ought: Evolutionary origins of great ape intelli- Tomasello, M., & Call, J. (1997). Primate cognition, New York: gence. pp. 122–139. Cambridge, UK: Cambridge University Oxford University Press. Press. Tomasello, M., Call, J., & Hare, B. (1998). Five primate species Santos, L. R., Rosati, A., Sproul, C., Spaulding, B., & Hauser, follow the visual gaze of conspecifi cs. Animal Behaviour, 55, M. D. (2005). Means-end tool choice in cotton-top tamarins 1063–1069. (Saguinus oedipus): fi nding the limits on primates’ knowledge Uehara, S. (1997) Predation on mammals by the chimpanzee of tools. Animal Cognition, 8, 236–246. (Pan troglodytes). Primates, 38– 193–214. Sanz, C., Call, J., & Morgan, D. (2009). Design complexity in Vander Wall, S. B. (1990). Food hoarding in animals, Chicago: termite-fi shing tools of chimpanzees (Pan troglodytes). Biology University of Chicago Press. Letters, 5, 293–296. van Essen, D. C., Anderson, C. H., & Felleman, D. J. (1992). Schino, G., Tiddi, B., & Di Sorrentino, E. P. (2006). Information processing in the primate visual system an inte- Simultaneous classifi cation by rank and kinship in Japanese grated systems perspective. Science, 255, 419–423. macaques. Animal Behaviour, 71, 1069–1074. van Horik, J., & Burns, K. C. (2007). Cache spacing patterns Schloegl, C., Kotrschal, K., & Bugnyar, T. (2007). Gaze follow- and reciprocal cache theft in New Zealand robins. Animal ing in common ravens, Corvus corax: ontogeny and habitua- Behaviour, 73, 1043–1049. tion. Animal Behaviour, 74, 769–778. van Lawick-Goodall, J. (1968). Th e behaviour of free-living Seed, A., Emery, N. J., & Clayton, N. S. (2009a). Intelligence chimpanzees in the Gombe Stream reserve. Animal Behaviour in corvids and apes: A case of convergent evolution? Ethology, Monographs, 1, 161–311. 115, 401–420. van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, Seed, A. M., Call, J., Emery, N. J., & Clayton, N. S. (2009b) C. D., Singleton, I., Suzuki, A., Utami, S. S., & Merrill, M. Chimpanzees solve the trap problem when the confound (2003). Orangutan cultures and the evolution of material of tool-use is removed. Journal of Experimental Psychology - culture. Science, 299, 102–105. Animal Behavior Processes, 35, 23–34. van Schaik, C. P., Deaner, R. O., & Merrill, M. Y. (1999). Th e Seed, A. M., Clayton, N. S., & Emery, N. J. (2007). Postconfl ict conditions for tool use in primates: implications for the evo- third-party affi liation in rooks, Corvus frugilegus. Current lution of material culture. Journal of Human Evolution, 36, Biology, 17, 152–158. 719–741. Seyfarth, R. M., & Cheney, D. L. (1984). Grooming, alliances von Bayern, A. M. P., de Kort, S. R., Clayton, N. S., & Emery, and reciprocal altruism in vervet monkeys. Nature, 308, N. J. (2007). Th e role of food- and object-sharing in the 541–543. development of social bonds in juvenile jackdaws (Corvus Shettleworth, S. J. (2010). Cognition, Evolution and Behaviour. monedula). Behaviour, 144, 711–733. New York: Oxford University Press. von Bayern, A. M. P., & Emery, N. J. (2009). Jackdaws respond Silk, J. B. (1999). Male bonnet macaques use information to human attentional states and communicative cues in dif- about third-party rank relationships to recruit allies. Animal ferent contexts. Current Biology, 19, 602–606. Behaviour, 58, 45–51. Wallace, A. R. (2000). Th e Malay Archipelago, Singapore: Oey. Smolker, R. A., Richards, A. F., Connor, R. C., & Pepper, J. Watanabe, S., & Clayton, N. S. (2007). Observational visu- W. (1992). Sex-diff erences in patterns of association among ospatial encoding of the cache locations of others by western Indian-ocean bottle-nosed dolphins. Behaviour, 123, scrub-jays (Aphelocoma californica). Journal of Ethology, 25, 38–69. 271–279.

100 convergent evolution of cognition in corvids, apes and other animals

005_Vonk_Ch05.indd5_Vonk_Ch05.indd 110000 110/18/20110/18/2011 88:15:13:15:13 PPMM OUP UNCORRECTED PROOF – FIRST-PROOF, 10/18/11, NEWGEN

Watts, D. P. (1998). Coalitionary mate guarding by male chim- Wrangham, R. W. (1999). Evolution of coalitionary killing. panzees at Ngogo, Kibale National Park, Uganda. Behavioral Yearbook of physical anthropology. New York: Wiley-Liss. Ecology and Sociobiology, 44, 43–55. Yosef, R., & Yosef, N. (2009). Cooperative hunting in Weir, A. A. S., Chappell, J., & Kacelnik, A. (2002). Shaping of brown-necked ravens (Corvus rufficollis) on Egyptian hooks in new Caledonian crows. Science, 297, 981–981. Mastiguve (Uromastyx aegyptius). Journal of Ethology, 28, Whiten, A., & Byrne, R. W. (1988). Tactical deception in pri- 385–388. mates. Behavioral and Brain Sciences, 11, 233–244. Zinkivskay, A., Nazir, F., & Smulders, T. V. (2009). What-Where- Wursig, B., & Wursig, M. (1980). Behavior and ecology of When memory in magpies (Pica pica). Animal Cognition, 12, the dusky dolphin, Lagenorhynchus obscurus, in the South- 119–125. Atlantic. Fishery Bulletin, 77, 871–890.

van horik, clayton, emery 101

005_Vonk_Ch05.indd5_Vonk_Ch05.indd 110101 110/18/20110/18/2011 88:15:13:15:13 PPMM