Effects of sun compass error on spatial search by Clark's nutcrackers.

Animals employ compasses during navigation, but little attention has been paid to how accuracy is maintained in the face of compass error, which is inevitable in biological systems. The use of multiple landmarks may minimize the effect of compass error. We allowed Clark's nutcrackers to cache seeds in an outdoor aviary with either one or four landmarks present, and subsequently subjected them to small clock-shifts mimicking the effects of compass error. As predicted, the results showed a significant decrease in search accuracy following the clock-shift when one landmark was present but not when four landmarks were present. These results support that nutcrackers encode information from the sun as well as terrestrial landmarks, and these spatial cues are used in a flexible manner. Overall, our results are important as they support the hypothesis that multiple landmarks may be used during situations where the sun compass has even a small amount of error.

Cognition-mediated evolution of low-quality floral nectars.

Plants pollinated by hummingbirds or bats produce dilute nectars even though these animals prefer more concentrated sugar solutions. This mismatch is an unsolved evolutionary paradox. Here we show that lower quality, or more dilute, nectars evolve when the strength of preferring larger quantities or higher qualities of nectar diminishes as magnitudes of the physical stimuli increase. In a virtual evolution experiment conducted in the tropical rainforest, bats visited computer-automated flowers with simulated genomes that evolved relatively dilute nectars. Simulations replicated this evolution only when value functions, which relate the physical stimuli to subjective sensations, were nonlinear. Selection also depended on the supply/demand ratio; bats selected for more dilute nectar when competition for food was higher. We predict such a pattern to generally occur when decision-makers consider multiple value dimensions simultaneously, and increases of psychological value are not fully proportional to increases in physical magnitude.

Context-dependent seed dispersal by a scatter-hoarding corvid.

Corvids (crows, jays, magpies and nutcrackers) are important dispersers of large-seeded plants. Studies on captive or supplemented birds suggest that they flexibly adjust their scatter-hoarding behaviour to the context of social dynamics and relative seed availability. Because many corvid-dispersed trees show high annual variation in seed production, context-dependent foraging can have strong effects on natural corvid scatter-hoarding behaviour. We investigated how seed availability and social dynamics affected scatter-hoarding in the island scrub jays (Aphelocoma insularis). We quantified rates of scatter-hoarding behaviour and territorial defence of 26 colour-marked birds over a three-year period with variable acorn crops. We tested whether caching parameters were correlated with variation in annual seed production of oaks as predicted by the predator dispersal hypothesis, which states that caching rates and distances should vary with seed abundance in ways that benefit tree fitness. We also tested whether antagonistic interactions with conspecifics would affect scatter-hoarding adversely, as found in experimental studies. Caching behaviour varied with acorn availability. Caching distances correlated positively with annual acorn crop size, increasing by as much as 40% between years. Caching rates declined over time in years with small acorn crops, but increased when crops were large. Acorn foraging and caching rates were also negatively correlated with rates of territorial aggression. Overall foraging rates, however, were not associated with aggression, suggesting that reduced dispersal rates were not simply due to time constraints. Our field results support laboratory findings that caching rates and distances by scatter-hoarding corvids are context-dependent. Furthermore, our results are consistent with predictions of the predator dispersal hypothesis and suggest that large seed crops and social interactions among scatter-hoarders affect dispersal benefits for oaks and other masting tree species.

Visual search and attention in blue jays (Cyanocitta cristata): Associative cuing and sequential priming.

Visual search for complex natural targets requires focal attention, either cued by predictive stimulus associations or primed by a representation of the most recently detected target. Because both processes can focus visual attention, cuing and priming were compared in an operant search task to evaluate their relative impacts on performance and to determine the nature of their interaction in combined treatments. Blue jays were trained to search for pairs of alternative targets among distractors. Informative or ambiguous color cues were provided before each trial, and targets were presented either in homogeneous blocked sequences or in constrained random order. Initial task acquisition was facilitated by priming in general, but was significantly retarded when targets were both cued and primed, indicating that the two processes interfered with each other during training. At asymptote, attentional effects were manifested mainly in inhibition, increasing latency in miscued trials and decreasing accuracy on primed trials following an unexpected target switch. A combination of cuing and priming was found to interfere with performance in such unexpected trials, apparently a result of the limited capacity of working memory. Because the ecological factors that promote priming or cuing are rather disparate, it is not clear whether they ever simultaneously contribute to natural predatory search.

Direct and relational representation during transitive list linking in pinyon jays (Gymnorhinus cyanocephalus).

The authors used the list-linking procedure (Treichler & Van Tilburg, 1996) to explore the processes by which animals assemble cognitive structures from fragmentary and often contradictory data. Pinyon jays (Gymnorhinus cyanocephalus) were trained to a high level of accuracy on 2 implicit transitive lists, A > B > C > D > E and 1 > 2 > 3 > 4 > 5. They were then given linkage training on E > 1, the single pair that linked the 2 lists into a composite, 10-item hierarchy. Following linkage training, the birds were tested on nonadjacent probe pairs drawn both from within (B-D and 2-4) and between (D-1, E-2, B-2, C-3) each original list. Linkage training resulted in a significant transitory disruption in performance, and the adjustment to the resulting implicit hierarchy was far from instantaneous. Detailed analysis of the course of the disruption and its subsequent recovery provided important insights into the roles of direct and relational encoding in implicit hierarchies.

Changing room cues reduces the effects of proactive interference in Clark's Nutcrackers, Nucifraga columbiana.

To determine what factors are important for minimizing interference effects in spatial memory, Clark's Nutcrackers, Nucifraga columbiana were tested for their spatial memory for two serial lists of locations per day. In this experiment two unique landmark sets were either different between List 1 and List 2 or the same. We found that Nutcrackers were most susceptible to interference when the landmark sets were the same. This study suggests that repeatedly testing animal memory in the same room, with the same cues, can hamper recall due to interference.

Differences in relative hippocampus volume and number of hippocampus neurons among five corvid species.

The relative size of the avian hippocampus (Hp) has been shown to be related to spatial memory and food storing in two avian families, the parids and corvids. Basil et al. [Brain Behav Evol 1996;47:156-164] examined North American food-storing birds in the corvid family and found that Clark's nutcrackers had a larger relative Hp than pinyon jays and Western scrub jays. These results correlated with the nutcracker's better performance on most spatial memory tasks and their strong reliance on stored food in the wild. However, Pravosudov and de Kort [Brain Behav Evol 2006;67:1-9] raised questions about the methodology used in the 1996 study, specifically the use of paraffin as an embedding material and recalculation for shrinkage. Therefore, we measured relative Hp volume using gelatin as the embedding material in four North American species of food-storing corvids (Clark's nutcrackers, pinyon jays, Western scrub jays and blue jays) and one Eurasian corvid that stores little to no food (azure-winged magpies). Although there was a significant overall effect of species on relative Hp volume among the five species, subsequent tests found only one pairwise difference, blue jays having a larger Hp than the azure-winged magpies. We also examined the relative size of the septum in the five species. Although Shiflett et al. [J Neurobiol 2002;51:215-222] found a difference in relative septum volume amongst three species of parids that correlated with storing food, we did not find significant differences amongst the five species in relative septum. Finally, we calculated the number of neurons in the Hp relative to body mass in the five species and found statistically significant differences, some of which are in accord with the adaptive specialization hypothesis and some are not.

Do Clark's nutcrackers demonstrate what-where-when memory on a cache-recovery task?

What-where-when (WWW) memory during cache recovery was investigated in six Clark's nutcrackers. During caching, both red- and blue-colored pine seeds were cached by the birds in holes filled with sand. Either a short (3 day) retention interval (RI) or a long (9 day) RI was followed by a recovery session during which caches were replaced with either a single seed or wooden bead depending upon the color of the cache and length of the retention interval. Knowledge of what was in the cache (seed or bead), where it was located, and when the cache had been made (3 or 9 days ago) were the three WWW memory components under investigation. Birds recovered items (bead or seed) at above chance levels, demonstrating accurate spatial memory. They also recovered seeds more than beads after the long RI, but not after the short RI, when they recovered seeds and beads equally often. The differential recovery after the long RI demonstrates that nutcrackers may have the capacity for WWW memory during this task, but it is not clear why it was influenced by RI duration.

Cognitive representation in transitive inference: a comparison of four corvid species.

During operant transitive inference experiments, subjects are trained on adjacent stimulus pairs in an implicit linear hierarchy in which responses to higher ranked stimuli are rewarded. Two contrasting forms of cognitive representation are often used to explain resulting choice behavior. Associative representation is based on memory for the reward history of each stimulus. Relational representation depends on memory for the context in which stimuli have been presented. Natural history characteristics that require accurate configural memory, such as social complexity or reliance on cached food, should tend to promote greater use of relational representation. To test this hypothesis, four corvid species with contrasting natural histories were trained on the transitive inference task: pinyon jays, Gymnorhinus cyanocephalus; Clark's nutcrackers, Nucifraga columbiana; azure-winged magpies, Cyanopica cyanus; and western scrub jays, Aphelocoma californica. A simplified computer model of associative representation displayed a characteristic pattern of accuracy as a function of position in the hierarchy. Analysis of the deviation of each subject's performance from this predicted pattern yielded an index of reliance on relational representation. Regression of index scores against rankings of social complexity and caching reliance indicated that both traits were significantly and independently associated with greater use of relational representation.

What scatter-hoarding animals have taught us about small-scale navigation.

Many animals use cues for small-scale navigation, including beacons, landmarks, compasses and geometric properties. Scatter-hoarding animals are a unique system to study small-scale navigation. They have to remember and relocate many individual spatial locations, be fairly accurate in their searching and have to remember these locations for long stretches of time. In this article, we review what is known about cue use in both scatter-hoarding birds and rodents. We discuss the importance of local versus global cues, the encoding of bearings and geometric rules, the use of external compasses such as the Sun and the influence of the shape of experimental enclosures in relocating caches or hidden food. Scatter-hoarding animals are highly flexible in how and what they encode. There also appear to be differences in what scatter-hoarding birds and rodents encode, as well as what scatter-hoarding animals in general encode compared with other animals. Areas for future research with scatter-hoarding animals are discussed in light of what is currently known.

Landmark use by Clark's nutcrackers (Nucifraga columbiana): influence of disorientation and cue rotation on distance and direction estimates.

Many species have been shown to encode multiple sources of information to orient. To examine what kinds of information animals use to locate a goal we manipulated cue rotation, cue availability, and inertial orientation when the food-storing Clark's nutcracker (Nucifraga columbiana) was searching for a hidden goal in a circular arena. Three groups of birds were used, each with a different goal-landmark distance. As the distance between the goal and the landmark increased, nutcrackers were less accurate in finding the correct direction to the goal than they were at estimating the distance (Experiment 1). To further examine what cues the birds were using to calculate direction, the featural cues within the environment were rotated by 90 degrees and the birds were either oriented when searching (Experiments 2 and 3) or disoriented (Experiment 3). In Experiment 4, all distinctive visual cues were removed (both internal and external to the environment), a novel point of entry was used and the birds were either oriented or disoriented. We found that disorienting the nutcrackers so that they could not use inertial cues did not influence the birds' total search error. The birds relied heavily but not completely on cues within the environment, as rotating available cues caused them to systematically shift their search behavior. In addition, the birds also relied to some extent on Earth-based cues. These results show the flexible nature of cue use by the Clark's nutcracker. Our study shows how multiple sources of spatial information may be important for extracting multiple bearings for navigation.

The synthetic approach to the study of spatial memory: have we properly addressed Tinbergen's "four questions"?

In 1963, Niko Tinbergen suggested that to truly understand the behavior of an animal, the ultimate causes (e.g., adaptive value, evolutionary history) as well as the proximate mechanisms (e.g., neurobiology, development) that result in the production of the behavior must be understood in an integrated framework. We examine whether the study of spatial memory in food storing birds has adequately addressed Tinbergen's questions and highlight the work of Sara Shettleworth, who has made a tremendous contribution to this area of study, and whom this issue honors. Our conclusion is that while the study of food caching and spatial memory in birds has been a very good model of a program of research that has addressed Tinbergen's questions, additional work remains.

Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica).

In serial reversal learning, subjects learn to respond differentially to 2 stimuli. When the task is fully acquired, reward contingencies are reversed, requiring the subject to relearn the altered associations. This alternation of acquisition and reversal can be repeated many times, and the ability of a species to adapt to this regimen has been considered as an indication of behavioral flexibility. Serial reversal learning of 2-choice discriminations was contrasted in 3 related species of North American corvids: pinyon jays (Gymnorhinus cyanocephalus), which are highly social; Clark's nutcrackers (Nucifraga columbiana), which are relatively solitary but specialized for spatial memory; and western scrub jays (Aphelocoma californica), which are ecological generalists. Pinyon jays displayed significantly lower error rates than did nutcrackers or scrub jays after reversal of reward contingencies for both spatial and color stimuli. The effect was most apparent in the 1st session following each reversal and did not reflect species differences in the rate of initial discrimination learning. All 3 species improved their performance over successive reversals and showed significant transfer between color and spatial tasks, suggesting a generalized learning strategy. The results are consistent with an evolutionary association between behavioral flexibility and social complexity.

Pigeons and people select efficient routes when solving a one-way "traveling salesperson" task.

The authors presented people (Experiment 1) and pigeons (Experiments 2 and 3) with a large number of 1-way traveling salesperson problems that consisted of 3, 4, and 5 identical stimuli (nodes) on a computer monitor. The sequence of nodes that each traveler selected was recorded, and the distance of the route was subsequently determined. The routes the pigeons and people selected were reliably more efficient than those used by a Monte Carlo model given the same problems. The pigeons' routes were significantly less efficient than a nearest neighbor model of performance, however. In Experiment 3, pigeons were required to select a route that was within the top 33% of all possible solutions for a given problem. The pigeons' solutions were significantly more efficient than those observed in Experiment 2, in which the behavioral criterion was not imposed. The mechanisms that pigeons and people may have been using to solve the traveling salesperson problems are discussed.

Interference effects in the memory for serially presented locations in Clark's nutcrackers, Nucifraga columbiana.

The authors tested the spatial memory of serially presented locations in Clark's nutcrackers (Nucifraga columbiana). Birds were serially presented with locations in an open room. The authors buried a seed in a sand-filled cup at each location and then tested nutcrackers for their memory for each location in the list by using the cluster method. For each item in the list, the authors opened a cluster of 6 holes. Accuracy was measured by how many tries were required for the bird to find the correct location within each cluster. In Experiments 1 and 2, the authors presented 2 lists of locations and found evidence for proactive and retroactive interference. Nutcrackers made errors by visiting the interfering list of locations during recovery of the target list. This finding demonstrates that nutcrackers are susceptible to proactive and retroactive interference during the recall of spatial information.

Spatial heterogeneity, predator cognition, and the evolution of color polymorphism in virtual prey.

Cryptically colored prey species are often polymorphic, occurring in multiple distinctive pattern variants. Visual predators promote such phenotypic variation through apostatic selection, in which they attack more abundant prey types disproportionately often. In heterogeneous environments, disruptive selection to match the coloration of disparate habitat patches could also produce polymorphism, but how apostatic and disruptive selection interact in these circumstances is unknown. Here we report the first controlled selection experiment on the evolution of prey coloration on heterogeneous backgrounds, in which blue jays (Cyanocitta cristata) searched for digital moths on mixtures of dark and light patches at three different scales of heterogeneity. As predicted by ecological theory, coarse-grained backgrounds produced a functional dimorphism of specialists on the two patch types; fine-grained backgrounds produced generalists. The searching strategies of the jays also varied with the habitat configuration, however. Complex backgrounds with many moth-like features elicited a slow, serial search that depended heavily on selective attention. The result was increased apostatic selection, producing a broad range of moth phenotypes. Backgrounds with larger, more uniform patches allowed the birds to focus on the currently most rewarding patch type and to search entire patches rapidly in parallel. The result was less apostatic selection and lower phenotypic variability. The evolution of polymorphism in camouflaged prey depends on a complex interaction between habitat structure and predator cognition.

The fine-grained spatial abilities of three seed-caching corvids.

We used a psychophysical method to examine the ability of three corvid species to discern fine-grained spatial information. Nutcrackers, pinyon jays, and scrub-jays were required to discriminate the distance between two landmarks on a computer screen in an operant chamber. All three species were able to discriminate between arrays that differed by 20 mm; the discrimination gradients for scrub-jays and pinyon jays were sharper than those for nutcrackers, however. The results suggest that differences in spatial memory among these species are not related to differences in fine-grained perception.

Clark's nutcrackers (Nucifraga columbiana) and the effects of goal--landmark distance on overshadowing.

Three groups of Clark's nutcrackers (Nucifraga columbiana) were trained to find a goal location defined by an array of 4 landmarks that varied in goal--landmark distance. The arrays for each group differed in the distance of the closest landmark and contained goal--landmark distances that were common across groups, allowing for the examination of the effects of both relative and absolute goal--landmark distance on encoding of a landmark array. All 3 groups readily learned the task and were subsequently tested in probe tests with only single landmarks from the array available. Search error in tests with single landmarks was compared both within and across groups. Results demonstrated that both relative and absolute goal-landmark distances are important in spatial search.

Pinyon jays use transitive inference to predict social dominance.

Living in large, stable social groups is often considered to favour the evolution of enhanced cognitive abilities, such as recognizing group members, tracking their social status and inferring relationships among them. An individual's place in the social order can be learned through direct interactions with others, but conflicts can be time-consuming and even injurious. Because the number of possible pairwise interactions increases rapidly with group size, members of large social groups will benefit if they can make judgments about relationships on the basis of indirect evidence. Transitive reasoning should therefore be particularly important for social individuals, allowing assessment of relationships from observations of interactions among others. Although a variety of studies have suggested that transitive inference may be used in social settings, the phenomenon has not been demonstrated under controlled conditions in animals. Here we show that highly social pinyon jays (Gymnorhinus cyanocephalus) draw sophisticated inferences about their own dominance status relative to that of strangers that they have observed interacting with known individuals. These results directly demonstrate that animals use transitive inference in social settings and imply that such cognitive capabilities are widespread among social species.