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The Cognitive Animal Empirical and Theoretical Perspectives on Animal Cognition This PDF includes a chapter from the following book: The Cognitive Animal Empirical and Theoretical Perspectives on Animal Cognition © 2002 Massachusetts Institute of Technology License Terms: Made available under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International Public License https://creativecommons.org/licenses/by-nc-nd/4.0/ OA Funding Provided By: The open access edition of this book was made possible by generous funding from Arcadia—a charitable fund of Lisbet Rausing and Peter Baldwin. The title-level DOI for this work is: doi:10.7551/mitpress/1885.001.0001 Downloaded from http://direct.mit.edu/books/edited-volume/chapter-pdf/677490/9780262268028_c001600.pdf by guest on 29 September 2021 17 Spatial and Social Cognition in Corvids: An Evolutionary Approach Russell P. Balda and Alan C. Kamil research plan using controlled laboratory ex- Research Questions periments and captive birds. Fortunately, nut- crackers are quite willing to cache and recover The central research questions that have guided seeds in laboratory settings and do so with a high our studies since 1981 combine issues and tech- degree of accuracy, both in a sandy floor indoors niques from both comparative psychology and (Balda 1980; Balda and Turek 1984) or out of avian ecology. Most of our questions originate doors (Vander Wall 1982), as well as in a room from the cognitive implications of extensive field with a raised floor containing sand-filled cups as studies on the natural history, ecology, and potential cache sites (Kamil and Balda 1985). behavior of seed-caching corvids. Because our The ability to study caching and cache recovery questions have evolved as our studies progressed, under controlled laboratory conditions allowed we have chosen to give a historical perspective us to test hypotheses on how the nutcrackers find outlining the progression of our ideas and ques- their caches. tions (see Shettleworth, chapter 16 in this volume For example, because we were able to control for a description of a similar program with seed- when and where the birds cached, we were able caching tits and chickadees). to rule out odor, marking the site, list learning, and site preferences (Kamil and Balda 1985). We Research Paradigm also learned that these birds remember some cache sites better than others and recover food Our research program began by examining the from the better-remembered sites first, and with amazing spatial memory system of the Clark’s greater accuracy (Kamil and Balda 1990a). Birds nutcracker (Nucifraga columbiana). A single sometimes revisit cache sites after they have nutcracker buries up to 33,000 food items in recovered the seeds. On these revisits they treat thousands of di¤erent subterranean sites and the cache site di¤erently than when they pre- retrieves them months later with a high degree of viously emptied it (Kamil et al. 1993). These accuracy. These birds are highly adapted for this birds also showed a long retention interval for behavior because they possess a strong, sharp bill cache memory, recovering caches with high for opening cones, extracting seeds, and burying levels of accuracy up to 9 months after creating them in the substrate; a sublingual pouch (Bock them (Balda and Kamil 1992). et al. 1973) for carrying large numbers of seeds The results of several studies showed that nut- (up to 90 pinyon pine, Pinus edulis, seeds); and crackers were using visual landmarks for accu- strong wings for carrying seeds great distances rate cache recovery (Vander Wall 1982; Balda (up to 22 km). Birds have been observed digging and Turek 1984). Data obtained by using a up seeds in the field with seemingly uncanny ac- clock-shift technique, popular in studies of mi- curacy (Vander Wall and Balda 1977, 1981; gratory birds and homing pigeons, suggest that Vander Wall and Hutchins 1983). Although this seed-caching corvids may use the sun as a com- behavior occurs regularly in the field, field con- pass under some circumstances (Wiltschko et al. ditions do not allow the design of studies to ad- 2000). Thus we successfully brought a behavior dress the questions of how nutcrackers are able prominent in the field into the laboratory, where to locate their stored food. we could examine it in great detail. From these Studies of the cognitive mechanisms involved studies we concluded that nutcrackers were using in cache recovery required the development of a Downloaded from http://direct.mit.edu/books/edited-volume/chapter-pdf/677490/9780262268028_c001600.pdf by guest on 29 September 2021 Russell P. Balda and Alan C. Kamil 130 a spatial memory system to recover their caches Specificity of Spatial Memory and that this system was of long duration and robust (Kamil and Balda 1990b). This di¤erence in the accuracy of cache recovery raises an interesting issue that is important in Comparative Studies understanding the evolution of cognitive abili- ties: Is this spatial memory restricted to remem- On the slopes of the San Francisco Peaks in bering where food has been stored or is it more Northern Arizona, five species of corvids cache general? Natural selection selects for outcomes, and recover seeds. These species di¤er in their not mechanisms. Thus it could be that the nut- degree of dependence on their seed caches to crackers’ ability is highly specific. On the other survive winter, as well as in their adaptations for hand, selection could have operated to sharpen this behavior. The Clark’s nutcracker is the most already existing spatial cognitive abilities, in highly specialized of these species and lives at which case nutcrackers should perform quite the highest elevations, where winters are harsh well on a variety of spatial tasks. Therefore, we and alternative foods are very scarce. At mid- embarked on a series of comparative studies elevations, moderately specialized Steller’s jays using di¤erent procedures to test spatial mem- (Cyanocitta stelleri) and pinyon jays (Gymno- ory. These included two- and three-dimensional rhinus cyanocephalus) coexist and also cache pine open-room analoges of the radial maze (Ka- seeds when they are available. Both species have mil et al. 1994; Balda et al. 1997) and operant a relatively sharp bill for extracting seeds and an nonmatching-to-sample tests. These studies all expandible esophagus for carrying pine seeds. A involved spatial memory, but not the recovery of pinyon jay may cache up to 26,000 pine seeds food previously cached. The results of these when cone crops are abundant (Balda 1987). At studies were consistent with our hypothesis. The lower elevations, the less specialized western species most dependent on seed caches for winter scrub jays (Aphelocoma californica) and Mexican survival performed at higher levels. If depen- jays (A. ultrimarina) cache and recover seeds dence on stored food has selected for improved much less intensely than the birds at higher spatial cognitive abilities, it has done so in a way elevations. Scrub and Mexican jays possess no that is not completely domain specific. morphological adaptations for the harvest, However, there is some specificity. Olson transport, caching, and recovery of seeds, and et al. (1995) tested three species in an operant the lower elevations where they live have mild nonmatching-to-sample test. In one experiment, winters and a year-round supply of arthropods, the birds were required to remember a spatial seeds, and berries. location; in another, a color. As in many other These di¤erences in natural history raise a experiments, the most seed-dependent species compelling question about evolution and cogni- performed best in the spatial test, showing tion. Are these di¤erences in morphological ad- much longer retention intervals. However, this aptations for food caching, and the concomitant di¤erence disappeared completely during the dependence on cached food, associated with dif- color test. This suggests a modularity for spatial ferences in the spatial cognitive abilities of these cognition. species? Are species that have the highest level of dependence on cached food also better at finding Social Cognition their caches? In a comparative test with three of these species, we found that although all three More recently, we have become interested in performed above chance, nutcrackers and pinyon extending our natural history-based analysis of jays recovered their caches more accurately than cognition to another domain. Primatologists western scrub jays (Balda and Kamil 1989). (e.g., Humphrey 1976) have developed a hy- Downloaded from http://direct.mit.edu/books/edited-volume/chapter-pdf/677490/9780262268028_c001600.pdf by guest on 29 September 2021 Spatial and Social Cognition in Corvids 131 pothesis about the evolution of intelligence based with many open holes for caching in the floor. on the cognitive demands of sociality. Animals The observer bird could view all areas of the that live in large, stable social groups must be floor. Later the observer was allowed to attempt able to assess the consequences of their behav- to recover the caches it had observed being iors, classify other animals as members of various made. While pinyon jays and Mexican jays groups and coalitions, and recognize and remem- recovered caches with an accuracy above chance ber traits of many other individuals. Success levels, nutcrackers did not perform above chance within the group will be improved if an individ- (Bedneko¤ and Balda 1996a,b). ual possesses a rich internal representation of the In another experiment, pinyon jays learning a group that will allow it to adjust to the fluid na- novel task were facilitated by being able to ob- ture of the group. These cognitive demands will serve a conspecific performing the same task, but necessarily increase as group size increases and nutcrackers were not so facilitated (Templeton can be expected to be greatest for those animals et al. 1999).
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