A test of the adaptive specialization hypothesis: Population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapilla).

Episodic Memory in Nonhuman Animals

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.

The effects of physostigmine and scopolamine on memory for food caches in the black-capped chickadee

The study of hybrid zones can provide insight into the genetic basis of species differences that are relevant for the maintenance of reproductive isolation. Hybrid zones can also provide insight into climate change, species distributions, and evolution. The hybrid zone between black-capped chickadees (Poecile atricapillus) and Carolina chickadees (Poecile carolinensis) is shifting northward in response to increasing winter temperatures but is not increasing in width. This pattern indicates strong selection against chickadees with admixed genomes. Using high-resolution genomic data, we identified regions of the genomes that are outliers in both time points and do not introgress between the species; these regions may be involved in the maintenance of reproductive isolation. Genes involved in metabolic regulation processes were overrepresented in this dataset. Several gene ontology categories were also temporally consistent-including glutamate signaling, synaptic transmission, and catabolic processes-but the nucleotide variants leading to this pattern were not. Our results support recent findings that hybrids between black-capped and Carolina chickadees have higher basal metabolic rates than either parental species and suffer spatial memory and problem-solving deficits. Metabolic breakdown, as well as spatial memory and problem-solving, in hybrid chickadees may act as strong postzygotic isolation mechanisms in this moving hybrid zone.

Urbanization has been shown to affect the physiological, morphological, and behavioral traits of animals, but it is less clear how cognitive traits are affected. Urban habitats contain artificial food sources, such as bird feeders that are known to impact foraging behaviors. As of yet, however, it is not well known whether urbanization and the abundance of supplemental food during the winter affect caching behaviors and spatial memory in scatter hoarders. We aim to compare caching intensity and spatial memory performance along an urban gradient to determine (i) whether individuals from more urbanized sites cache less frequently and perform less accurately on a spatial memory task, and (ii) for the first time in individual scatter hoarders, whether slower explorers perform more accurately than faster explorers on a spatial memory task. We assessed food caching, exploration of a novel environment, and spatial memory performance of wild-caught black-capped chickadees (Poecile atricapillus; N = 95) from 14 sites along an urban gradient. Although the individuals that cached most in captivity were all from less urbanized sites, we found no clear evidence that caching intensity and spatial memory accuracy differed along an urban gradient. At the individual level, we found no significant relationship between spatial memory performance and exploration score. However, individuals that performed more accurately on the spatial task also tended to cache more, pointing to a specialization of spatial memory in scatter hoarders that could occur at the level of the individual, in addition to the previously documented specialization at the population and species levels.

The three-way association among food-storing behavior, spatial memory, and hippocampal enlargement in some species of birds is widely cited as an example of a new ‘cognitive ecology’ or ‘neuroecology.’ Whether this relationship is as strong as it first appears and whether it might be evidence for an adaptive specialization of memory and hippocampus in food-storers have recently been the subject of some controversy [Bolhuis and Macphail, 2001; Macphail and Bolhuis, 2001]. These critiques are based on misconceptions about the nature of adaptive specializations in cognition, misconceptions about the uniformity of results to be expected from applying the comparative method to data from a wide range of species, and a narrow view of what kinds of cognitive adaptations are theoretically interesting. New analyses of why food-storers (black-capped chickadees, Poecile atricapilla) respond preferentially to spatial over color cues when both are relevant in a memory task show that this reflects a relative superiority of spatial memory as compared to memory for color rather than exceptional spatial attention or spatial discrimination ability. New studies of chickadees from more or less harsh winter climates also support the adaptive specialization hypothesis and suggest that within-species comparisons may be especially valuable for unraveling details of the relationships among ecology, memory, and brain in food-storing species.

Food storage by black-capped chickadees: Memory for the location and contents of caches

No latitudinal differences in adrenocortical stress response in wintering black-capped chickadees (Poecile atricapilla)

In seasonally variable environments, enhanced cognitive abilities may allow animals to adjust their behavior to changing conditions. Nonmigratory food-caching birds, like chickadees, rely on specialized spatial cognition to successfully cache and retrieve food items and survive the winter. Previous studies have linked spatial cognitive performance in chickadees to enhanced fitness, including survival and reproduction; however, it remains unknown whether females assess male cognitive ability via direct observation or secondary sexual traits. In this study, we investigated whether variation in common secondary sexual traits of songbirds, song and plumage, serve as indicators of cognitive ability in black-capped chickadees (Poecile atricapillus) when accounting for dominance rank. To explore this, we brought wild male black-capped chickadees into captivity, tested their performance in three spatial cognitive abilities (spatial learning, cognitive flexibility, and long-term retention), determined the relative social dominance ranks among all individuals, measured plumage reflectance in six body regions, and recorded their fee-bee songs to assess the relationship between these variables. Our findings show that birds with brighter white plumage and greater contrast between black and white plumage patches showed better spatial learning and memory performance. In contrast, we found no significant associations between cognitive performance and song variation. Our results suggest that females may use some secondary sexual traits as signals for cognitive performance, although, we suggest direct observation may also be important for mate choice involving cognitive ability in chickadees. This work provides insights into female mating decisions, highlighting the complex nature of sexual selection and female preferences.

Environmental variability, the value of information, and learning in winter residents

Recovery of cached sunflower seeds by Black-capped Chickadees (Parus atricapillus) was observed in four laboratory experiments. Results of the first experiment were consistent with the hypothesis that chickadees use spatial memory to recover seeds cached 24 h earlier. The second experiment demonstrated that individuals have a high recovery rate for their own caches and a low recovery rate for caches made by another. The third and fourth experiments demonstrated that one chickadee observing another caching seeds provided no recovery benefit to the observer in comparison to its performance when recovering seeds hidden in its absence. This result held for 2-h and for 6-min delays between observation and attempted recovery. We believe that spatial memory is used by chickadees, that the individual carrying out the caching has a large recovery advantage over a conspecific that searches the same patch, and that the perceptual and motor experience involved in the act of traveling to a cache location may be necessary for the establishment of spatial memory.

Black-capped chickadees and other food-storing birds recover their scattered caches by remembering the spatial locations of cache sites. Bilateral hippocampal aspiration reduced the accuracy of cache recovery by chickadees to the chance rate, but it did not reduce the amount of caching or the number of attempts to recover caches. In a second experiment, hippocampal aspiration dissociated performance of a task requiring memory for places from performance of a task requiring memory for cues associated with food, disrupting the former but not the latter

Sex, estradiol, and spatial memory in a food-caching corvid

Many animals use spatial memory. Although much work has examined the accuracy of spatial memory, few studies have explicitly focused on its longevity. The importance of long-term spatial memory for foraging has been demonstrated in several cases. However, the importance of such long-term memory for all animals is unclear. In this study, we present the first evidence that a parid species (the black-capped chickadee, Poecile atricapillus) can remember the location of a single food item for at least 6months under an associative-learning spatial memory paradigm with multiple reinforcements. We did not detect a significant difference in memory longevity between two populations of chickadees shown previously to differ in short-term spatial memory and hippocampal morphology, an area of the brain involved in spatial memory. Our study showed that small birds such as parids can maintain spatial memories for long periods, a feat shown previously only in corvids. Moreover, we were able to demonstrate this longevity within the context of only 16 repeated trials. We speculate that this ability may potentially be useful in relocating caches if reinforced by repeated visits. Future studies are necessary to test whether our results were specifically due to multiple reinforcements of the food-containing location and whether parids may have similar memory longevity during food-caching experiences in the wild.

Following development, the avian brain continues to produce neurons throughout adulthood, which functionally integrate throughout the telencephalon, including the hippocampus. In food-storing birds like the black-capped chickadee (Poecile atricapillus), new neurons incorporated into the hippocampus are hypothesized to play a role in spatial learning. Previous results on the relation between hippocampal neurogenesis and spatial learning, however, are correlational. In this study, we experimentally suppressed hippocampal neuronal recruitment and tested for subsequent effects on spatial learning in adult chickadees. After chickadees exhibited significant learning, we treated birds with daily injections of either saline or methylazoxymethanol (MAM), a toxin that suppresses cell proliferation in the brain and monitored subsequent spatial learning. MAM treatment significantly reduced cell proliferation around the lateral ventricles and neuronal recruitment in the hippocampus, measured using the cell birth marker bromodeoxyuridine. MAM-treated birds performed significantly worse than controls on the spatial learning task 12 days following the initiation of MAM treatment, a time when new neurons would begin functionally integrating into the hippocampus. This difference in learning, however, was limited to a single trial. MAM treatment did not affect any measure of body condition, suggesting learning impairments were not a product of non-specific adverse effects of MAM. This is the first evidence of a potential causal link between hippocampal neurogenesis and spatial learning in birds.