S16.5: Exploration and curiosity in birds: Functions and mechanisms
Hans Winkler1 & Bernd Leisler2
1Konrad Lorenz-Institut für Vergleichende Verhaltensforschung der Österreichischen Akademie der Wissenschaften, Savoyenstraße 1A, A-1160 Wien, Austria, fax 43 1 486 2121 28, firstname.lastname@example.org; 2, Forschungsstelle für Ornithologie der Max-Planck-Gesellschaft, Vogelwarte Radolfzell, Schlossallee 2, D-78315 Radolfzell-Möggingen, Germany, e-mail email@example.com. Winkler, H. & Leisler, B. 1999. Exploration and curiosity in birds: Functions and mechanisms. In: Adams, N.J. & Slotow, R.H. (eds) Proc. 22 Int. Ornithol. Congr., Durban: 915-932. Johannesburg: BirdLife South Africa.
Exploration constitutes an important component of avian behaviour. Yet, it is largely ignored by many ornithologists studying the function and adaptation of behaviour. Non-task oriented behaviour has mainly been studied by psychologists interested in motivation and learning usually using primates and rodents. In this review we present various examples of exploratory behaviour in birds. Generally, exploratory behaviour has been insufficiently described, its adaptive value is often implied but rarely studied, and field studies are almost completely lacking. We define exploration as any activity which takes up time, which does not satisfy immediate needs, and which serves to obtain information. Our examples come from different aspects of ecologically relevant behaviour. Experiments with reed warblers suggest that they show unrewarded activity and that this activity is clearly related to habitat and morphology and influenced by novelty. Further experiments with reed warblers and other species indicate that the various parameters commonly associated with exploratory behaviour, neophobia, duration and intensity of exploration, and curiosity, are independent constituents of exploration. Novelty, the difference between past experience and current perception, may relate to all aspects in the environment. Comparative studies with parrots showed that exploratory behaviour is related to food type, habitat and migratory behaviour, among other things. In parrots there also exists a clear relationship with social hierarchy, dominant individuals access novel objects first and they defend them against other conspecifics. Finally, we discuss other examples of exploratory behaviour and provide a framework for the study of the adaptive value of exploration. The key issues in this context are the value of information and environmental uncertainty. From these we derive predictions relating environment and exploratory behaviour which could be tested in comparative studies.
Exploration and curiosity are undoubtedly important components of bird behaviour. The phenomena subsumed under these headings are diverse, and they are relevant for many aspects of behaviours.
Since there is no unified theory of exploration and curiosity, data and relevant hypotheses are scattered among many studies motivated by a wide range of problems and effectuated in many different methodological contexts. The contributions to this symposium reflect this diversity to some extent. Most studies of curiosity involve mammals, notably rodents and primates. Nevertheless, behaviour perceived as curiosity driven or exploratory by researchers is widespread among birds. Ornithologists have perhaps more often invoked exploration to explain unexpected observations or experimental results than they have studied it on its own right. As a result of birds diverse life style and the vast information known about their behaviour, ecology and evolution, birds are ideal subjects for the study of exploration and its ultimate function.
Exploration in a wide sense encompasses any behaviour that results in growth of knowledge. This implies that learning is invariably linked with exploration (Welker 1961, Renner 1990). Indeed, if one views learning as information gathering (see Stephens 1993), then one can define exploration as any activity that promotes learning.
Since information can be taken up in the course of any activity, it is sometimes difficult to circumscribe exploration. Foraging birds, for example, would benefit from learning while pursuing a policy of rate maximisation in terms of energy, or they could gather information by deviating from optimal behaviour deliberately. They also could encounter some novel stimuli as consequence of their failure to pursue the optimal policy perfectly (Rechten et al. 1983, Shettleworth 1988).
The question whether there exist activities, which use up time in which the bird satisfies no immediate needs, and which function as information gathering (Renner 1990) remains a central issue in the study of exploration. If information is gathered in the course of an activity not primarily or exclusively devoted to gain knowledge, we talk about extrinsic or accidental information gathering. We will apply the term exploration when information gathering is intrinsic to the observed behaviour, and particularly, if this information is of no value for immediate consumption (food etc.).
MODES OF EXPLORATION
Many studies involving mammals and birds equate exploration with exploration of space, and with locomotory behaviour. One of the widely used techniques is the open-field test, which has serious drawbacks (Renner 1990) and will not be discussed here. Birds need spatial information especially in the context of territorial behaviour, homing and navigation, and food caching.
Manipulation and inspection
An important part of exploration is to investigate and manipulate objects. This includes exploration of food, nest material, tools, predators, companions and potential mates. Birds manipulate objects with their feet and bill while they forage, feed, or construct a nest or bower, and when they are using any kind of tool. Exploration may involve the same activities. Additionally, objects can be inspected from a distance. A brief glance at an object may suffice to convince a bird of its state or quality, a possibility that poses great methodological difficulties for empirical studies.
During object exploration birds acquire knowledge about features of new objects or familiar objects containing new properties, and develop specialised skills to deal with them.
Play (object, locomotory, social play) seems to be widespread among birds (Ficken 1977, Smith 1983, Ortega & Bekoff 1987, Caro 1988). Play often consists of incomplete behaviour, may be a mixture of normally separate activities, and often is exaggerated and repetitive (Ficken 1977). It is often difficult to distinguish the various activities birds may show during exploration or play, for instance, exploring birds may also interact with objects repeatedly. Therefore, we will include examples of playful behaviour in our discussion as well.
THE FUNCTION OF EXPLORATORY BEHAVIOUR
The literature hardly touches the question of the function of exploration. If authors refer to function, statements as a rule are vague and general (Barnett 1958, Barnett & Cowan 1976, Anderson 1986, Renner 1990). Yoerg (1991) considered possible relationships between ecology and cognition but without particularly referring to exploration. Glickman & Sroges (1966) in their broad comparative study of zoo animals attempted to formulate some expectations about the ecological aspects of exploration. Little has been done to specify ecological conditions in which exploration should be most important, and the obvious variation among species in exploratory behaviour remains unexplained (e.g. Heth et al. 1987, Poucet et al. 1988, Cowan 1977a, Glickman & Hartz 1964, D'Udine et al. 1987, Birke et al. 1985, Frynta 1992).
Value of information
Some important progress was made after biologists adopted the concept of the value of information formulated by Gould (1974) for the economic sciences. In short, the value of information is measured as the difference between the outcome of a decision made by an informed individual compared to an uninformed one. It is obvious that in an environment, which does not contain any regularity it does not pay to strive for knowledge. Then simple rules may be best (Wolf & Hainsworth 1986). But, events often can be predicted on account of preceding events, daylight and seasons are cyclic, and there is order in spatial arrangements, and, birds are able to detect and to take advantage of such regularities (Biebach et al. 1989, Gwinner 1999). In a completely predictably universe information has no value.
Neither in a completely stable nor in an unpredictably changing environment does it pay to continue to collect information once it had been established that the environment happens to be in either of these extremes states. If the environment stays stable over a very long period compared to the generation time of the bird, an innate program may substitute initial information gathering completely.
The costs of exploratory behaviour may be equated to the time and energy lost for other, ultimately more rewarding, activities and to the inherent dangers of object exploration (e.g. poisons), risk of injury or harassment from social partners or potential mates, and of venturing into unknown space. Costs of exploration grow with the presence of predators or with exposure to harsh physical conditions.
A special form of exploration, namely sampling or environmental tracking, has received some attention (Stephens 1987, Stephens & Krebs 1986). The situation modelled is one, in which there is one food source of stable quality and another one that varies between good and bad states stochastically. The state of the stable source lies between the two possible states of the alternating one. The problem addressed is, when and how often should a forager sample the state of the variable source. For the sampling problem, theory is advanced and has even outrun data (Shettleworth 1988). The experimental results on birds (Great Tits Parus major, pigeons, hummingbirds, woodpeckers) largely confirm the predictions of the models at least qualitatively (Lima 1984, Dow & Lea 1987, Krebs et al. 1978, Tamm 1987, Shettleworth et al. 1988). Hummingbirds and Great Tits sampled more frequently than expected in some situations (Plowright & Plowright 1987, Tamm 1987).
Birds optimally foraging in a benign environment would specialise on the most profitable food types (Stephens & Krebs 1986). Hence, extrinsic uptake of information would be restricted in rich environments, and only poor environments would foster learning. Juvenile Yellow-eyed Juncos Junco phaeonotus continue to feed and handle large mealworms although they are less profitable than small ones. This persistence appears to increase their foraging efficiency in the long run, since adults can handle large mealworms much better which reverses relative profitability of small versus large ones (Sullivan 1988).
A special case of food manipulation, namely the opening of nuts or shells has been treated theoretically as well as empirically. The theory (McNamara & Houston 1985) concerns food items, which have to be manipulated before the reward is procured, and which vary in the time needed to obtain the reward. The information accumulated in the course of manipulation is used to update the expectation of the further time required for success. To decide how this information is applied depends on existing knowledge about the variability among items. If no information is available the a priori assumption of a constant reward rate is plausible. In that situation, it is never optimal to give up before a reward is found and one would expect high persistency (McNamara & Houston 1985).
Experiments and observations on the shell dropping of gulls (Zach 1979) and the seed opening of Bullfinches Pyrrhula pyrrhula support the predicted persistence for cases in which food reward is certain and the time until success is variable (Greig-Smith 1987). Unclear is yet how the birds obtain information about environmental variation. We conjecture that if food items potentially vary substantial in handling times, naive birds should also explore many different objects very persistently to arrive at good estimates of the variance in food accessibility. Support for this idea comes from Mettkes (1993, 1995) study on parrots. Species that include nuts in their diet explored novel objects especially long.
For other forms of object manipulation no such highly formalised hypothesis exist. But, one can assume that analogous principles work. Lengthy exploration should ensue in all cases in which success may occur after a very long time. Success could mean obtaining food, but also discovering a new value or use for the object. Manipulation of simple objects by juvenile and immature Keas Nestor notabilis may last for hours and birds do not habituate over successive days (Kubat 1992). The especially exploratory Worm-eating Warbler Helmitheros vermivorus spends about half of the time in experimental trials exploring unrewarding objects. This exploring behaviour does not decrease with trial number (Greenberg 1987a). Raptors and fish eating birds, will strike at and manipulate dead prey and inanimate objects; they will drop them and catch them in the air, for long periods (up to one hour). The repetitive character of this behaviour is characteristic. Turquoise-browed Motmots Eumomota superciliosa swallow pieces of food several times, regurgitate it, and continue to manipulate it (Smith 1977). When corvids, especially Ravens Corvus corax, manipulate objects they often combine this with conspicuous locomotory activities (Ficken 1977, Gwinner 1966). Australian Magpies Gymnorhina tibicen (Pellis 1981) and many parrots behave similarly.
Mangrove Finches Cactospiza heliobates of the Galápagos Islands mainly hunt for hidden prey often using also little sticks or thorns to probe holes, crevices and the like. They will also use their tools in unpromising locations (Curio & Kramer 1964). The even more specialised Woodpecker Finches Cactospiza pallida of the Galápagos are also very inquisitive and inspect every nook and surface of their environment. And, they show significant manipulative abilities beyond those of its tool use. They, like Mangrove Finches, do occasionally probe into cracks containing no food (Millikan & Bowman 1967).
Islands seem to provide several interesting examples for extreme feeding skills and exploration. Mainland Asian reed warblers Acrocephalus spp. are habitat and foraging specialists (Leisler et al. 1997). Island forms (A. mendanae, A. atypha, A. caffer) feed on a wider spectrum of prey types (crustaceans, lizards and geckos) than mainland species and use complex behaviour for prey handling (Bruner 1974), including techniques not exhibited at all by mainland species. Besides, the island species (A. mendanae, A. atypha) are recorded to be inquisitive and fearless (Holyoak 1973, Bruner 1974). In corvids, the omnivorous New Caledonian Crow Corvus moneduloides uses hooked sticks to probe into holes in living and dead trees, under bark, and among bases of large leaves (Hunt 1996). Another common feature of island birds is that they often feed on the ground and search for hidden food. That may also be part of their broadened niche and/or a consequence of resource distribution and reduced predation risk. Examples are the Keas, island populations of the Scrub Jay Aphelocoma caerulescens (Yeaton 1974), The Tuamotu Warbler Acrocephalus atypha (Bruner 1974), the inquisitive Galapagos mockingbirds (Bowman & Carter 1971, BL pers. obs.), and many of the Galapagos finches (Bowman 1961, Curio & Kramer 1964, Grant 1986).
Habitat selection is a combined result of various processes, among which there may be exploration (Hutto 1985) though innate preferences for some structures may play a role (Grünberger & Leisler 1993). Exploration of habitats should be favoured when habitats are not widely separated and birds can actually explore alternatives and are able to keep track of their relative profitability through sampling. Migrants and species well suited for low-cost long distance travel may be in a better position to adopt a sampling scheme (Hutto 1985).
Mettke (1993, 1995) studied neophobia in 61 species of parrots. The latency to approach a familiar food dish in the presence of a novel object correlated with ecological variables: Latencies between introduction of a novel object into the cage and first tactile contact through the bird where shortest in species which inhabit forest edge and in island species.
Evidence for effects of novelty in habitat selection come from the work by Ley (1988) on Acrocephalus warblers. Generally, warblers obtained from the wild explore unrewarded experimental chambers which differ only with respect to simple features (vertical versus horizontal perches) according to their natural habitat and morphology (Leisler et al. 1989). Groups of Reed Warblers A. scirpaceus and, respectively, Marsh Warblers A. palustris were raised in two separate habitat types (vertical vs. horizontal perches). Birds of each group preferred in later tests the habitat type they had not encountered before. After they had become familiar with the experimental situation, they behaved like birds caught in the wild. This effect of novelty may be an important mechanism for conquering new habitats and thus may functionally ensure that birds are not trapped in one particular habitat type.
Early experience exerts a strong influence on habitat preferences of adult birds (Glück 1984, Grünberger & Leisler 1993, Glück & Leisler 1994). How it is affected by the natal environment and early exploration is, however, little understood.
Site fidelity and territory
Habitat choice may be related with juvenile dispersal. In birds, juvenile dispersal has received little attention, although this is a period of high mortality, and is, especially when viewed as a phase of exploration, decisive for lifetime reproductive success. Most functional explanations so far centred on the population-ecological consequences of dispersal. But, it is obvious that post-fledging movements relate to exploratory behaviour. Birds explore an area to locate a breeding site or they establish navigational targets (Baker 1993). Evidence for the first comes, for instance, from translocation experiments with Flycatchers Ficedula sp. and Chaffinches Fringilla coelebs (Löhrl 1959, Berndt & Winkel 1980 and references therein, Sokolov et al. 1984). A Navigational target is the area a bird is familiar with, e.g. a breeding site. The farther a bird migrates, the more navigational errors will accumulate during the way back. Hence, the area explored should be larger in long distance migrants. Analyses of ringing data seem to confirm these ideas (Baker 1993).
Knowledge of space is important in many contexts (Metzgar 1967, Ambrose 1972, Stamps 1987). Yasukawa (1979) found that male Red-winged Blackbirds Agelaius phoeniceus which had successfully acquired a territory had visited the area at least a year before. In Collared Flycatchers Ficedula albicollis benefits of prior local experience seem to increase with age, and Pärt (1995) suggests, that males are the sex with the highest average search costs of finding nest sites and would, therefore, benefit most from local familiarity. Wild Turkeys Meleagris gallopavo which cover a greater area in exploratory movements before nesting are able to acquire better nesting habitats (Badyaev et al. 1996). Cinnamon Hummingbirds Amazilia rutila spend less time on their territory if its productivity is low (Gass & Montgomerie 1981), presumably exploring elsewhere. Female Turkeys start exploring after nest depredation. Females that sample larger areas are more successful later (Badyaev et al. 1996).
Mobbing is a notable behaviour associated with predators. Among the many different functions of mobbing discussed in the literature is cultural transmission of the characters of a predator (Curio 1978, Curio et al. 1978). The alarm calls uttered by mobbing birds and distress calls of a victim attract others to join the mobbing crowd. When mobbers follow and approach a predator they are able to learn basic features of their enemy. The attractiveness of spishing, used by field ornithologists (Davies 1987, Bauer 1989), for some species may be correlated with this type of exploration. The roughly similar predator inspection behaviour in fish (Pitcher et al. 1986) seems to be a much clearer case of information gathering about the current state of a predator.
Birds in groups have shown to exhibit less neophobia than solitary ones (Coleman & Mellgren 1994). Young American Kestrels play Falco sparverius simultaneously with similar intensity, and prefer the same play objects, when kept in a group (Negro et al. 1996). These general effects aside, hierarchically organised groups offer the opportunity to learn more about the costs and benefits of exploration. Dominant individuals can control the rewards of exploration by either transferring their risk to subordinates, reap the benefits conveyed through information gathered by others, or do all the exploring themselves.
Katzir's (1982) study of Jackdaws Corvus monedula showed that dominant individuals let subordinates investigate new space first, before they take over. Generally, dominants occupy safe sites (e.g. Koivula et al. 1994), and it is conceivable that in situations in which the risks of exploration are relatively high, particularly for an experienced bird, dominants would refrain from exploring. After information has been collected and has proven to be valuable, dominants easily can take over. For example, milk bottle opening Great Tits acquire this habit rather fortuitously and independent of rank, but only dominants are able to collect the benefits (Kothbauer-Hellmann 1990). Jackdaws do not easily detect food hidden under objects (e.g. under experimental mussel shells) on their own, but immediately make use of such sources independent of rank if they have the opportunity to watch familiar conspecifics uncovering the food. If, however, risk is low and possible benefits high, dominants may take over right away. In Ravens, the most dominant individual is the first to approach a novel object, and the other birds follow in an exploratory avalanche (Heinrich 1988). Naïve Willow tits Parus montanus also may take advantage of experienced and dominant birds, and approach novel food faster with an experienced partner (Mönkkönen & Koivula 1993). In Keas dominance on unrewarded familiar or novel objects was closely correlated with dominance on food (Kubat 1992): in both situations the most dominant birds tried to monopolise the object or food. This seems to be a general pattern among parrots as a study of 23 species showed. Dominant parrots were more likely to be the first to approach a novel object, made earlier contact with it and explored longer than subdominant individuals (Mettke 1993). For the dominant Jackdaws risks of exploration appear to be probably higher than the expected relative gain, whereas lower ranking birds may gain from new resources out of reach of the dominant more than enough to compensate for that risk (Katzir 1982). To acquire new resources, on the other hand, is most important for Ravens and Keas. The dominant male that is able to provide food both for the female and the young can leave the group and wins breeding status.
Much work centers on novelty as stimulus quality (e.g. Berlyne 1950, Welker 1961, Corey 1978). Novelty is a function of any discrepancy between past experience and present sensation (Corey 1978). The term novelty is most appropriate if a new (or completely forgotten) condition of the environment is encountered. Eventually novel objects cease to elicit exploratory responses when presented repeatedly (e.g. Berlyne 1950, Renner 1990): exploratory behaviour transforms novelty to familiarity (McReynolds 1962), and, as Fagen (1981) remarks, exploration is not repeated unless something changes.
The experimental work of Franchina & Dyer (1989) on domestic chicks suggests that novelty is truly a general stimulus property that can be separated from specific stimulus characteristics like colour and taste. They experimentally created aversion against novel visual or taste cues and showed that this aversion was transferred to novel taste, respectively, visual stimuli.
Novelty also has been discussed in relation to certain stimulus characteristics. Studies on the evolution of warning colours showed that it is not easy to discern whether a prey item is conspicuous because of its background contrast, its novelty, or because of specific preferences or aversions (Coppinger 1969, 1970, Roper & Cook 1989). Novelty alone can not account for the experimental results (Smith 1983, Roper & Cook 1989, Roper 1990), and the related assumption that novel conspicuous prey morphs attract more attention and hence foster predator learning has not yet been tested thoroughly (Endler 1991). However, the general effect of novelty on memorability seems to be a well established fact (Shettleworth 1972, Guilford & Dawkins 1991).
It is often difficult to distinguish between an odd and a conspicuous object (Mueller 1968). A known object in an array of other familiar and similar objects may represent a novel situation. Keas, for instance, react virtually as strongly to a familiar, but odd, object as they do to new objects (Kubat 1992).
Novelty is a strong stimulus, seemingly independent of the quality of the cues associated with it (Heinrich 1995). As more information about is acquired, the quality of the explored entity becomes more important. Circumstantial evidence that innate preferences may shape exploratory behaviour does not only derive from data on habitat selection, but also from work on object exploration. Keas explore objects of a certain consistency for longer (e.g. hide versus plastic, Kubat 1992), and Ravens soon develop preferences for edible items (Heinrich 1995). Naive, hand raised juvenile Worm-eating Warblers prefer to manipulate dead and curled leaves (Greenberg 1987a), in which they search for arthropods in the wintering grounds (Greenberg 1987b). Fledglings of the American Kestrel mainly play with objects that resemble their habitual prey (Negro et al. 1996). Bristle-thighed Curlews Numenius tahitiensis chicks slam various items, including lichen, moss, and seaweed against the ground. Adults confine this behaviour to food items. They also may slam stones against large eggs to open them (Marks & Hall 1992).
Novelty is just one aspect of environmental uncertainty. To show that birds respond to uncertainty per se is very difficult, but would be of outmost importance for the study of the mechanisms and function of exploration.
Motivation and cognition are what (comparative) psychologists are mainly interested in (e.g. Berlyne 1966, Inglis 1983, Renner 1990) and the majority of studies concentrates on rodents and primates. Exploration, as unrewarded behaviour (we exclude here the possibilty that exploration is rewarding per se), is little distinguished from rewarded activities (e.g. Timberlake 1983) and both activities may be closely associated (Pellis 1981). This raises an important methodological problem especially for field studies, because it may be impossible to distinguish foraging from exploratory behaviour.
Although the concept of curiosity is central to the study of motivation, it poses many difficulties as just few examples show. Curiosity is a mechanism that serves in approaching new objects. Neophilia and neophobia are related concepts and are observable as responses of animals toward novel situations. The motivation of exploratory behaviour, however, can not be fully explained with the neophilia-neophobia continuum (Murphy 1978). Exploration itself may be governed by cues that are different from those that elicited it. And, neophobia is not necessarily equivalent or related to fear (Misslin & Cigrang 1986, Hilakivi & Lister 1990). Latencies to approach a novel object placed in a neutral location and latencies to approach a food dish with a novel object close by did not correlate among parrot species (Mettke 1993). Neophobia, measured as hesitancy to feed on unfamiliar food, is a function of gender, genetic and experiential factors in Domestic Chicks (Jones 1986).
Information-primacy theory is an interesting approach to the problem of the motivation of exploration. It posits that behaviour is primarily guided by an innate tendency to reduce environmental uncertainty through exploration (Inglis 1983, Inglis & Ferguson 1986, Inglis & Shepherd 1994). Only if immediate needs have to be satisfied, the animal would reduce exploration, the primary drive. Because an animal looks for moderate uncertainties during foraging it will explore and use many different food sources learning about them in the course of these activities (Forkman 1993). Birds should prefer mildly novel stimuli according to the optimal rate of information processing they can achieve (McReynolds 1962).
The effects of hunger and satiation on exploration have been treated in quite a few rodent studies and have been studied in birds as well. Some birds seem to explore less and some explore more when hungry. Nestling Reed Warblers play with objects when satiated, when fledged they explore their environment right after feeding and a 10-minutes period of resting and preening (Davies & Green 1976). Turquoise-browed Motmots showed playful sequences of food manipulation only when satiated (Smith 1977). Hungry domestic hens appear to be less ready to acquire general environmental information (Nicol & Pope 1993), and hungry Ravens do not respond to novel objects (Heinrich 1988), however, the likelihood that adult Ravens would explore increases with resource scarcity (Heinrich 1995). Starlings Sturnus vulgaris gradually shift to feeding on an easily accessible food source with increasing food deprivation, without giving up searching for hidden food totally (Inglis & Ferguson 1986). Similarly, Worm-eating Warblers do not give up to visit unrewarded objects when they are deprived of food and alternative objects are rewarded (Greenberg 1987a). The most inquisitive of the Galapagos Mockingbirds Nesomimus trifasciatus macdonaldi increases exploration of natural and artificial egg-shaped objects when fasting (Bowman & Carter 1971). Likewise, Woodpecker Finches of the Galápagos procure more tools when hungry (Millikan & Bowman 1967). Object play correlates well with foraging in Australian Magpies while social play does not (Pellis 1981). Hungry Keas manipulate wooden cubes more persistently than satiated ones (Ritzmeier & Winkler 1994). New experiments with canaries Serinus canaria (Ritzmeier & Winkler 1997) showed that in this species as well object manipulation increases with food deprivation. However, as experiments on latent inhibition showed, hungry birds did not learn about these objects.
Exploratory and coping style are also intimately related to aggressiveness (Verbeek et al. 1996) and are discussed in detail by Drent & Marchetti (1999).
In a large number of species differences in foraging skills between young and adult birds have been found (see Wunderle 1991 for an extensive review, Marchetti & Price 1989). Many of the relevant studies also demonstrated that juveniles rarely perform activities that require well developed skills. How juveniles become more skilled and knowledgeable with age, particularly when they rarely perform the respective behavioural acts, is little known. Often it is not clear to what degree the observed improvement in proficiency with age is due to learning and specific exploratory behaviour, or to higher mortality of the less dextrous (Wunderle 1991). In the Large Cactus Finch Geospiza conirostris those individuals more likely to survive have acquired skills to procure insect larvae dwelling under bark or in opuntia pads (Grant & Grant 1989). Great differences in the ability to retain food resources between age classes imply, among other things, that a long period of learning, and possibly active exploration, is necessary. This is the case with the curious and inquisitive Kea (Diamond & Bond 1989, 1991). Object play, and social play are more common in fledglings of raptor species hunting agile prey (birds, mammals) and in those species with more elaborate hunting techniques (Bustamante 1999).
The idea that juvenile and adult birds differ with respect to their responses to novel stimuli is central to Greenbergs Neophobia Threshold Hypothesis (Greenberg 1990, 1999). Clear indications of a special juvenile phase of exploratory activities is provided through observations on Australian Magpies in which object exploration and social play peak 4-6 weeks after fledging (Pellis 1981). In the development of foraging skills of Reed Warblers, flycatching matures independently from specific experience, whereas mandibulating the prey is learned within a short period (Davies & Green 1976). Woodpecker Finches develop individual styles of tool-use, which suggests that individual experience in a juvenile phase of intensive learning and exploration is important (Millikan & Bowman 1967). Adult American Kestrels would not manipulate objects, while fledglings of this species readily engage in playful activities (Negro et al. 1996).
There are only few species of birds of which we know that show intense inquisitive behaviour through adult life. Playful manipulation of objects seems to be a major preoccupation in the life of Keas and is not restricted to juveniles (Diamond & Bond 1989). At least in captivity, woodpeckers, parrots, and corvids manipulate and experiment with sticks and other objects independent of age (pers. obs., M. Ficken 1977). These observations, however, need to be confirmed with quantitative data. Ravens retain neophilia to some degree at least to their first year (Heinrich 1995).
Comparative psychologists have devoted some effort to investigate the effects of early deprivation. If mammals are socially deprived of varied stimulation during early stages of ontogeny, this has pronounced effects on later object exploration (Einon & Morgan 1976, Gardner et al. 1975, Mason 1984, Renner 1987). Rodent studies also showed that perceptual deprivation results not only in reduced spatial exploration, but also retards the performance in discrimination tasks and maze learning (Greenough et al. 1972).
Studies and concern about environmental enrichment is almost exclusively devoted to mammals. This bias is hard to understand and may rest on the assumption that birds are deemed to be less intelligent. The few studies available nevertheless show that one can observe similar effects in birds as in mammals and suggest that environmental enrichment is an important aspect of bird welfare (King 1999).
Chicks from enriched environments are less timid to enter novel space and accept novel food more readily (Jones 1982, 1986). Moustached Warblers Acrocephalus melanopogon hand-raised in an environment which only contained simple perches differed in various aspects of their behaviour from birds whose environment contained additional structures as wood-wool, rolls of paper, and strings (Raach & Leisler 1989). They showed more neophobia, measured as latency to approach a food dish in the presence of a novel object suspended over it, and were less apt in procuring food from structures made from wire. The frequency of approaching novel objects and the duration of interactions with them did not differ. Grünberger & Leisler conducted similar experiments with Coal Tits Parus ater (Grünberger & Leisler 1990, Grünberger 1992). They raised a group of these birds in an environment containing a few perches and some paper rolls only, and they enriched the cages of an experimental group with assorted artificial objects like ropes, brooms, and flower pots. Birds from the enriched environment exhibited less neophobia. From these results one can conclude that the birds beyond getting familiar with particular objects form some sort of expectations about the richness of the environment and about the probability of encounters with novel situations.
It is obvious that a great deal of research is still needed in practically all aspects of avian exploratory behaviour. Even some very basic questions, for example how to distinguish true exploratory behaviour from other activities, have not been answered satisfactorily. If we assume that exploratory behaviour is adaptive, it seems plausible to expect differences among closely related species in accordance with their ecology. We also have a pressing need for theoretical studies on information use and on the function of exploration. So many facets of exploratory behaviour and curiosity need more research that it is difficult to emphasise just few of them.
One of the difficulties in comparing the results of various authors has been that exploration was measured in many different ways. However, the latency to approach a novel object or to enter unknown space and the duration of exploration may measure very different aspects. Very rarely it was confirmed that during an activity assumed to be exploratory information has been picked up by the animal.
Poor environments should favour extrinsic information gathering. Foragers exploiting patches optimally should stay longer in patches in poor environments, thus gaining precise estimates of resource properties (Rodríguez- Gironés & Vásquez 1997). Since in poor environments diet breadth is higher, optimal diet choice (see above) would promote learning about a high variety of objects. In environments in which stretches of bad conditions are interspersed with periods of abundance, intrinsic exploration would be advantageous, because affluence retards extrinsic exploration. Particularly, if these periods of good supply coincide with the juvenile phase, a strong motivation for exploration is to be expected.
Highly mobile birds, such as migrants or others with the necessary prerequisites for long distance movements, should be more likely to explore alternative habitats (Hutto 1985). They also are frequently faced with novel situations, and possibly need to use information gained at stopover sites repeatedly.
Birds need advance information in planning future activities especially in those cases in which they are faced with several opportunities limited to short periods of time. Likely examples are males that seek extra-pair copulations (Schwagmeyer 1995), and female brood parasites that have to keep track of the breeding cycles of several individual hosts.
Much more information is needed about the costs of exploration. Analysis of the causes of mortality may yield information on the dangers involved in exploration. Johnson (1989), working with small mammals, cast the relation between predation and the exploration of space into a simple graphical model, which could be used for avian studies as well.
Exploration always involves a trade-off between the renunciation of a short-term gain and a long-term benefit. Consequently, the problem can be framed using a life-history approach. We would predict that a species with high r would give up exploration at an early age and explore little, whereas individuals of species with low intrinsic population growth and a relatively high longevity should explore much and up to a high age.
Especially in cases where field studies already have shown that there is an improvement with age in certain skills there should be made some effort to find out how much this observed improvement is due to individual learning or to better survival of more skilled individuals. If the role of learning is greatest in those birds in which breeding is delayed (Johnston 1981) then there should be an extensive period of intense specific exploration. Helping has been sometimes ascribed the function to acquire breeding experience, however, support for this notion is scarce (Komdeur 1996).
Stephens' (1993) prediction that birds should explore mainly those features of the environment, which show high within generation predictability, but are variable between generations, could be tested in the laboratory as well as in the field, and with comparative data.
Play in birds is widespread and bears many features of exploratory behaviour. Yet, there is still little known about its occurrence in the wild (Ficken 1977, Smith 1983, Ortega & Bekoff 1987, Düttmann et al. 1998). To understand its many possible functions (Fagen 1981) we need such data. Recently, Byers and Walker (1995) reviewed the motor training hypothesis, which states that the function of play is adaptive modification of the developing neuromuscular system. Cerebellar synaptogenesis and skeletal muscle fiber differentiation can be modified only during a short period of postnatal development. Indeed, in three mammal species, the age distribution of play matches the age distribution of the cerebellar synaptogenesis and the skeletal muscle fiber differentiation. Therefore, Byers and Walker concluded that play may not be motor training in the broad sense but rather be designed to affect specific types of development. Although the latter findings are restricted to mammalian species, we cannot exclude such primary benefits of play for altricial and precocial bird species as well.
Dealing with novelty and uncertainty is a significant aspect of the life of all birds. We hope that this contribution has shown, that much more attention should be paid to exploratory behaviour and that the study of birds promises fascinating insights.
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