Food-caching Mountain Chickadees Research Articles

What's in a mate? Social pairing decisions and spatial cognitive ability in food-caching mountain chickadees.

While researchers have investigated mating decisions for decades, gaps remain in our understanding of how behaviour influences social mate choice. We compared spatial cognitive performance and food caching propensity within social pairs of mountain chickadees inhabiting differentially harsh winter climates to understand how these measures contribute to social mate choice. Chickadees rely on specialized spatial cognitive abilities to recover food stores and survive harsh winters, and females can discriminate among males with varying spatial cognition. Because spatial cognition and caching propensity are critical for survival and likely heritable, pairing with a mate with such enhanced traits may provide indirect benefits to offspring. Comparing the behaviour of social mates, we found that spatial cognitive performance approached a significant correlation within pairs at low, but not at high elevation. We found no correlation within pairs in spatial reversal cognitive performance at either elevation; however, females at high elevation tended to perform better than their social mates. Finally, we found that caching propensity correlated within pairs at low, while males cached significantly more food than their social mates at high elevations. These results suggest that cognition and caching propensity may influence social mating decisions, but only in certain environments and for some aspects of cognition.

Food-caching mountain chickadees can learn abstract rules to solve a complex spatial-temporal pattern

The use of abstract rules in behavioral decisions is considered evidence of executive functions associated with higher-level cognition. Laboratory studies across taxa have shown that animals may be capable of learning abstract concepts, such as the relationships between items, but often use simpler cognitive abilities to solve tasks. Little is known about whether or how animals learn and use abstract rules in natural environments. Here, we tested whether wild, food-caching mountain chickadees (Poecile gambeli) could learn an abstract rule in a spatial-temporal task in which the location of a food reward rotated daily around an 8-feeder square spatial array for up to 34days. Chickadees initially searched for the daily food reward by visiting the most recently rewarding locations and then moving backward to visit previously rewarding feeders, using memory of previous locations. But by the end of the task, chickadees were more likely to search forward in the correct direction of rotation, moving away from the previously rewarding feeders. These results suggest that chickadees learned the direction rule for daily feeder rotation and used this to guide their decisions while searching for a food reward. Thus, chickadees appear to use an executive function to make decisions on a foraging-based task in the wild. VIDEO ABSTRACT.

Food-caching chickadees with specialized spatial cognition do not use scrounging as a stable strategy when learning a spatial task.

Social animals may use alternative strategies when foraging, with producer-scrounger being one stable dichotomy of strategies. While 'producers' search and discover new food sources, 'scroungers' obtain food discovered by producers. Previous work suggests that differences in cognitive abilities may influence tendencies toward being either a producer or a scrounger, but scrounging behaviour in the context of specialized cognitive abilities is less understood. We investigated whether food-caching mountain chickadees, which rely on spatial cognition to retrieve food caches, engage in scrounging when learning a spatial task. We analysed data from seven seasons of spatial cognition testing, using arrays of radio frequency identification-enabled bird feeders, to identify and quantify potential scrounging behaviour. Chickadees rarely engaged in scrounging, scrounging was not repeatable within individuals and nearly all scrounging events occurred before the bird learned the 'producer' strategy. Scrounging was less frequent in harsher winters, but adults scrounged more than juveniles, and birds at higher elevations scrounged more than chickadees at lower elevations. There was no clear association between spatial cognitive abilities and scrounging frequency. Overall, our study suggests that food-caching species with specialized spatial cognition do not use scrounging as a stable strategy when learning a spatial task, instead relying on learning abilities.

Natural variation in developmental condition has limited effect on spatial cognition in a wild food-caching bird.

Laboratory studies show that increased physiological burden during development results in cognitive impairment. In the wild, animals experience a wide range of developmental conditions, and it is critical to understand how variation in such conditions affects cognitive abilities later in life, especially in species that strongly depend on such abilities for survival. We tested whether variation in developmental condition is associated with differences in spatial cognitive abilities in wild food-caching mountain chickadees. Using tail feathers grown during development in juvenile birds, we measured feather corticosterone (Cortf) levels and growth rates and tested these birds during their first winter on two spatial learning tasks. In only 1 of the 3 years, higher feather Cortf was negatively associated with memory acquisition. No significant associations between feather Cortf and any other measurement of spatial cognition were detected in the other 2 years of the study or between feather growth rate and any measurement of cognition during the entire study. Our results suggest that in the wild, naturally existing variation in developmental condition has only a limited effect on spatial cognitive abilities, at least in a food-caching species. This suggests that there may be compensatory mechanisms to buffer specialized cognitive abilities against developmental perturbations.

Experimental manipulation of food distribution alters social networks and information transmission across environments in a food-caching bird

While many animals utilize socially transmitted information, there is still much to understand about how individuals form social networks and how these networks influence social information use. Here, we tested the hypothesis that food distribution and availability can influence social structure and social information transfer when discovering novel food sources. We experimentally manipulated distribution and access to food in wild food-caching mountain chickadees, Poecile gambeli , by randomly dividing existing individuals between two feeding locations, with birds only allowed to obtain food at one of the two locations. We carried out such manipulations at multiple sites associated with two montane elevations of different environmental harshness, where birds show differing use of social information. Following 2 weeks of manipulation, we measured social networks and then introduced novel feeders to test how the manipulation affected social information use. The manipulations effectively split the resident chickadees at both elevations into two distinct communities, and when subsequently discovering novel feeders, information transmission about novel food sources followed the new, rather than the premanipulation, network structure at both elevations, although low-elevation birds used social information more than high-elevation birds. Our data show that chickadees can quickly adjust their social associations in response to short-term changes in the distribution of available resources and that these changes influence who they learn from socially when searching for food. Overall, we observed that chickadees are highly flexible in their use of social information despite their rather stable social group structure and that this information use reflects the most current social environment that individuals experience. • Mountain chickadee social networks changed during short-term resource manipulation. • Social information transmission primarily followed the most recent network edges. • Birds at high elevations showed less social information transmission.

Social dominance has limited effects on spatial cognition in a wild food-caching bird.

Social dominance has long been used as a model to investigate social stress. However, many studies using such comparisons have been performed in captive environments. These environments may produce unnaturally high antagonistic interactions, exaggerating the stress of social subordination and any associated adverse consequences. One such adverse effect concerns impaired cognitive ability, often thought to be associated with social subordination. Here, we tested whether social dominance rank is associated with differences in spatial learning and memory, and in reversal spatial learning (flexibility) abilities in wild food-caching mountain chickadees at different montane elevations. Higher dominance rank was associated with higher spatial cognitive flexibility in harsh environments at higher elevations, but not at lower, milder elevations. By contrast, there were no consistent differences in spatial learning and memory ability associated with dominance rank. Our results suggest that spatial learning and memory ability in specialized food-caching species is a stable trait resilient to social influences. Spatial cognitive flexibility, on the other hand, appears to be more sensitive to environmental influences, including social dominance. These findings contradict those from laboratory studies and suggest that it is critical to investigate the biological consequences of social dominance under natural conditions.

Information maintenance of food sources is associated with environment, spatial cognition and age in a food-caching bird

Traditionally, exploration and exploitation of resources have been viewed as mutually exclusive behaviours in which animals can either allocate time to gathering information or to using known resources. But these behaviours can also be viewed as opposite ends of a continuum, with intermediate behaviours that balance exploration and exploitation, such as information maintenance. Updating previously acquired information through information maintenance can allow animals in unpredictable environments to track changing environmental conditions. Theoretical studies predict that the degree of involvement in information maintenance should depend on environmental predictability – when the overall environment is less predictable, animals should update previously acquired information more frequently because such information is less certain and could change quickly. We tested this hypothesis by allowing wild food-caching mountain chickadees, Poecile gambeli , to visit and sample multiple feeders with temporarily stable, unlimited food for five consecutive winters. We used an index of feeder use breadth to explore how feeder visits across multiple feeders varied with environmental conditions. Each feeder visit is associated with information updating, and more information maintenance should be associated with distributing more visits across more feeders. While controlling for the total number of visits by each individual, we found that (1) chickadees redistributed feeder use among more feeders when environmental conditions were harsh and unpredictable, (2) juveniles had a higher feeder use breadth than adults, and individuals reduced their feeder use breadth as they aged, (3) better spatial learning and memory ability but not spatial cognitive flexibility was associated with smaller feeder use breadth and (4) learning associated with decreased food availability reduced subsequent feeder use breadth. Our data supported our predictions that factors affecting the predictability of resource information (environmental conditions and individual characteristics such as cognition and age) affect how individuals engage in information maintenance. • Animals should update information more frequently when the environment is unpredictable. • Food-caching chickadees updated information about previously discovered food locations. • Chickadees updated food information more frequently in years with harsher winters. • Birds with better spatial cognition updated food information less. • Older birds with more experience updated food information less.

Specialized spatial cognition is associated with reduced cognitive senescence in a food-caching bird.

Senescence, the gradual reduction and loss of function as organisms age, is a widespread process that is especially pronounced in cognitive abilities. Senescence appears to have a genetic basis and can be affected by evolutionary processes. If cognitive senescence is shaped by natural selection, it may be linked with selection on cognitive abilities needed for survival and reproduction, such that species where fitness is directly related to cognitive abilities should evolve delayed cognitive senescence likely resulting in higher lifetime fitness. We used wild food-caching mountain chickadees, which rely on specialized spatial cognition to recover thousands of food caches annually, to test for cognitive senescence in spatial learning and memory and reversal spatial learning and memory abilities. We detected no signs of age-related senescence in spatial cognitive performance on either task in birds ranging from 1 to 6 years old; older birds actually performed better on spatial learning and memory tasks. Our results therefore suggest that cognitive senescence may be either delayed (potentially appearing after 6 years) or negligible in species with strong selection on cognitive abilities and that food-caching species may present a useful model to investigate mechanisms associated with cognitive senescence.

Elevation-related differences in annual survival of adult food-caching mountain chickadees are consistent with natural selection on spatial cognition

Animals inhabiting montane gradients experience varying winter climates that may result in differential selection on survival-related traits. Higher elevations in temperate climates are characterized by harsher winters with greater and longer-lasting snow cover compared to lower elevations, potentially leading to stronger selection for traits that improve fitness under these harsher conditions. For food-caching mountain chickadees, Poecile gambeli, inhabiting harsh high elevation environments, individual variation in spatial cognitive abilities related to cache retrieval is associated with significant differences in overwinter survival. Compared to lower elevations, stronger predicted selection on traits needed for overwinter survival at higher elevations can be expected to result in higher adult annual survival despite harsher environmental conditions, indicating that individuals that survive their first winter are better suited to survive similar subsequent selection events. Here, we used a Bayesian hierarchical Cormack-Jolly-Seber (CJS) model to estimate and compare survival of adult mountain chickadees at higher and lower elevations over 3 years. We showed that adult survival was consistently higher at higher elevations despite much harsher environmental conditions, supporting our hypothesis that selection on overwinter survival-related traits (such as spatial cognition) is stronger at our high elevation study area than at lower elevations. Understanding how environmental conditions are associated with different selection strengths on survival-related traits is an important question in behavioral ecology. Directly estimating differences in strength of selection is daunting, but comparing survival between environments may provide an alternative method. We tested for differences in adult survival in a resident food-caching species at higher and lower elevations varying in winter climate severity. These birds rely on food caches for winter survival, and juvenile birds with better spatial cognition (needed for cache retrieval) have higher survival during their first year at higher harsher elevations. Here, we report higher adult survival at higher elevations compared to lower elevations, despite much harsher winter environment. Such findings support our hypothesis for stronger selection in harsher winter conditions because individuals that survive their first year under stronger selection are better suited to survive subsequent selection events.

Elevation-related differences in the age structure of breeding birds suggest stronger selection at harsher elevations

How environmental variation affects the strength of selection is important for understanding phenotypic variation within a population. An indirect method to evaluate differences in selection pressures is to compare the age composition of a breeding population. A larger adult/first-year breeding ratio, due to higher juvenile mortality, may indicate stronger selection. We investigated the adult/first-year breeding ratios of food-caching mountain chickadees inhabiting different elevations. Chickadees at high elevations experience harsher winter conditions and cache more food items and have better spatial cognition to recover caches compared with their low-elevation counterparts. Cache recovery and spatial cognition are critical for overwinter survival and individuals with better spatial cognitive abilities are more likely to survive their first winter; therefore, these differences are likely a result of stronger selection pressures on spatial cognition and caching behavior at higher elevations. In support of this hypothesis, we found a significantly larger adult/first-year breeding ratio at high elevations compared with low elevations. This may suggest higher overwinter juvenile mortality and hence stronger selection pressures on survival-related traits at high elevations, consistent with elevation-related phenotypic differences. The strength of selection on survival-related traits varies across heterogenous environments. One way to assess the strength of selection is to measure the traits of individuals that are able to survive a particular selection event. Here we assessed the adult/first-year breeding ratios of resident, food-caching birds experiencing differentially harsh winter climates. These birds rely on spatial cognition to retrieve food caches and survive the winter; the largest annual selection event. At the individual level, those with better cognitive ability have demonstrated higher overwinter survival. However, at the population level, it remains unclear whether or not the strength of selection differs between harsh and mild winter climates. By assessing the age of breeders, we found a significantly larger adult/first-year breeding ratio in birds inhabiting harsher, high elevations compared with milder, low elevations. This suggests higher overwinter juvenile mortality and hence stronger selection pressures on survival-related traits at high elevations.

Natural Selection and Spatial Cognition in Wild Food-Caching Mountain Chickadees

Understanding how differences in cognition evolve is one of the critical goals in cognitive ecology [1-5]. In food-caching species that rely on memory to recover caches, enhanced spatial cognition has been hypothesized to evolve via natural selection [2, 6-8], but there has been no direct evidence of natural selection acting on spatial memory. Food-caching mountain chickadees living at harsher, higher elevations, with greater reliance on cached food have better spatial learning abilities and larger hippocampi containing more and larger neurons compared to birds from milder, lower elevations [9, 10]. Here, we tested for natural selection on spatial cognition in wild food-caching mountain chickadees at high elevations and documented the following: (1) compared to first-year juveniles, adults showed significantly better performance on two spatial cognitive tasks-spatial learning and memory and a consecutive reversal learning task; (2) cognitive performance in both spatial learning and reversal learning tasks was not significantly different between years in the same chickadees tested in their first year of life and after surviving to their second winter; and (3) cognitive performance in the spatial learning task was significantly better among the first-year juveniles that survived to their second winter compared to the subset of juveniles that did not survive. Taken together, our results provide evidence for natural selection on spatial cognition in a food-caching species living in harsh environments and suggest that natural selection associated with local environmental conditions might be generating intraspecific differences in cognitive abilities. VIDEO ABSTRACT.

Daily foraging routines in food-caching mountain chickadees are associated with variation in environmental harshness

Small birds overwintering in cold climates must meet the daily challenge of accumulating sufficient energy reserves throughout the day to ensure overnight survival. Theoretical work suggests that risk of starvation is a major force shaping optimal daily foraging routines. Animals are predicted to adjust how they distribute their daily foraging activity in relation to environmental harshness, which largely determines the risk of starvation. Here, we used radiofrequency identification (RFID)-enabled bird feeders to test whether mountain chickadees, Poecile gambeli – small, resident, food-caching birds – exhibited different daily foraging routines in harsher (higher elevation) versus milder (lower elevation) environments in the Sierra Nevada. In addition, we assessed foraging routines between four different periods of the nonbreeding season ranging from autumn (milder conditions) to winter and early spring (harsher conditions) and to late spring (milder conditions). We also tested whether individual variation in spatial cognition associated with food caching, which represents a more reliable food source that can be expected to lower risk of starvation, is associated with differences in daily foraging routines. Chickadees from both elevations distributed their daily foraging efforts differently throughout the nonbreeding season, consistent with theoretical predictions for milder and harsher conditions. Differences between chickadees from high and low elevations were especially pronounced during harsher winter periods, with chickadees from high elevations showing a bimodal daily routine, while low-elevation birds showed an inverted U-shaped daily routine, with most foraging during the middle of the day. Finally, significant differences in daily routines were associated with variation in spatial learning and memory performance. Overall, our study shows that daily foraging routines are consistent with risk of starvation under different degrees of environmental harshness, whether across nonbreeding seasons or between elevations, and that perception of harshness may be associated with cognitive abilities.

What makes specialized food-caching mountain chickadees successful city slickers?

Anthropogenic environments are a dominant feature of the modern world; therefore, understanding which traits allow animals to succeed in these urban environments is especially important. Overall, generalist species are thought to be most successful in urban environments, with better general cognition and less neophobia as suggested critical traits. It is less clear, however, which traits would be favoured in urban environments in highly specialized species. Here, we compared highly specialized food-caching mountain chickadees living in an urban environment (Reno, NV, USA) with those living in their natural environment to investigate what makes this species successful in the city. Using a 'common garden' paradigm, we found that urban mountain chickadees tended to explore a novel environment faster and moved more frequently, were better at novel problem-solving, had better long-term spatial memory retention and had a larger telencephalon volume compared with forest chickadees. There were no significant differences between urban and forest chickadees in neophobia, food-caching rates, spatial memory acquisition, hippocampus volume, or the total number of hippocampal neurons. Our results partially support the idea that some traits associated with behavioural flexibility and innovation are associated with successful establishment in urban environments, but differences in long-term spatial memory retention suggest that even this trait specialized for food-caching may be advantageous. Our results highlight the importance of environmental context, species biology, and temporal aspects of invasion in understanding how urban environments are associated with behavioural and cognitive phenotypes and suggest that there is likely no one suite of traits that makes urban animals successful.

Absence of population structure across elevational gradients despite large phenotypic variation in mountain chickadees (Poecile gambeli).

Montane habitats are characterized by predictably rapid heterogeneity along elevational gradients and are useful for investigating the consequences of environmental heterogeneity for local adaptation and population genetic structure. Food-caching mountain chickadees inhabit a continuous elevation gradient in the Sierra Nevada, and birds living at harsher, high elevations have better spatial memory ability and exhibit differences in male song structure and female mate preference compared to birds inhabiting milder, low elevations. While high elevation birds breed, on average, two weeks later than low elevation birds, the extent of gene flow between elevations is unknown. Despite phenotypic variation and indirect evidence for local adaptation, population genetic analyses based on 18 073 single nucleotide polymorphisms across three transects of high and low elevation populations provided no evidence for genetic differentiation. Analyses based on individual genotypes revealed no patterns of clustering, pairwise estimates of genetic differentiation (FST, Nei's D) were very low, and AMOVA revealed no evidence for genetic variation structured by transect or by low and high elevation sites within transects. In addition, we found no consistent evidence for strong parallel allele frequency divergence between low and high elevation sites within the three transects. Large elevation-related phenotypic variation may be maintained by strong selection despite gene flow and future work should focus on the mechanisms underlying such variation.

Predictably harsh environment is associated with reduced cognitive flexibility in wild food-caching mountain chickadees

Cognition is one of the mechanisms underlying behavioural flexibility, but flexibility of cognition itself may vary as a result of trade-offs between the ability to learn new information and the ability to retain old memories. How and when cognitive flexibility is constrained by this trade-off remains poorly understood. We investigated cognitive flexibility in wild food-caching mountain chickadees, Poecile gambeli, at different elevations experiencing different levels of environmental harshness during the nonbreeding season, using a spatial learning and memory reversal paradigm. There were no significant differences in sampling strategies between elevations, but high-elevation chickadees performed worse than low-elevation chickadees on the reversal task, indicating lower cognitive flexibility. Compared to the initial learning task, low-elevation chickadees improved their performance during the reversal task, while high-elevation chickadees performed worse. High-elevation birds inspected previously rewarding locations more frequently than other locations, suggesting that reduced cognitive flexibility is associated with proactive interference. Considering that high-elevation chickadees cache more food and are likely more dependent on these caches than their conspecifics from low elevation, and that chickadees from both elevations use similar sampling strategies, our findings suggest that stronger memories of more caches might interfere with acquisition and retention of new memories. Overall, our results suggest that predictably harsh environments might favour stronger memories at the expense of decreased cognitive flexibility, which is likely driven by increased proactive interference.

Individual variation in spatial memory performance in wild mountain chickadees from different elevations

For food-caching animals inhabiting environments with strong seasonal variation, harsh winter conditions may limit access to naturally available food and favour the evolution of enhanced spatial memory. Spatial memory enables animals to remember the locations of food caches for overwinter survival, therefore animals in harsher conditions may benefit more from more accurate spatial memory than conspecifics living under relatively mild conditions. Despite numerous laboratory studies lending indirect support to the hypothesis that a harsh environment favours the evolution of spatial memory, there is no direct evidence showing fitness consequences of variation in spatial memory. As a step towards evaluating this hypothesis in natural populations, we established spatial arrays of programmable bird feeders equipped with radio frequency identification technology (RFID) to test for individual variation in spatial memory in food-caching mountain chickadees, Poecile gambeli , at two elevations differing in winter climate severity. Individuals could only access food at a single rewarding feeder within an array of eight, and each individual had to learn the location of their unique rewarding feeder. Birds at higher elevations visited the arrays significantly more frequently than birds at lower elevations, suggesting more intense food caching. They also performed better at locating their rewarding feeder than birds from lower elevations. Individuals showing better performance participated in more overall trials, suggesting a link between food-caching propensity and memory performance, but higher overall levels of activity within each array yielded less accurate memory performance. Finally, rotating the arrays showed that birds relied specifically on spatial memory in order to locate their rewarding feeder. To our knowledge, this is the first explicit test of spatial memory performance in food-caching birds under natural conditions. Our results corroborate earlier laboratory-based work showing large individual variation in spatial memory performance and lay the groundwork for future investigation into the fitness consequences of individual variation and the evolution of spatial memory. • Harsh winters may favour the evolution of enhanced spatial memory in resident birds. • We tested spatial memory in chickadees from different elevations with radio frequency identification technology. • High-elevation birds outperformed low-elevation birds in a spatial memory task. • This is the first test of spatial memory variation in a food-caching bird in the wild.

Mountain chickadees from different elevations sing different songs: acoustic adaptation, temporal drift or signal of local adaptation?

Song in songbirds is widely thought to function in mate choice and male–male competition. Song is also phenotypically plastic and typically learned from local adults; therefore, it varies across geographical space and can serve as a cue for an individual's location of origin, with females commonly preferring males from their respective location. Geographical variation in song dialect may reflect acoustic adaptation to different environments and/or serve as a signal of local adaptation. In montane environments, environmental differences can occur over an elevation gradient, favouring local adaptations across small spatial scales. We tested whether food caching mountain chickadees, known to exhibit elevation-related differences in food caching intensity, spatial memory and the hippocampus, also sing different dialects despite continuous distribution and close proximity. Male songs were collected from high and low elevations at two different mountains (separated by 35 km) to test whether song differs between elevations and/or between adjacent populations at each mountain. Song structure varied significantly between high and low elevation adjacent populations from the same mountain and between populations from different mountains at the same elevations, despite a continuous distribution across each mountain slope. These results suggest that elevation-related differences in song structure in chickadees might serve as a signal for local adaptation.

Elevation-related differences in female mate preference in mountain chickadees: are smart chickadees choosier?

Heterogeneous environments are often associated with differential selection pressures favouring the evolution of local adaptations, and assortative mating is one of the mechanisms that might enhance such local adaptations. Montane environments present an example in which environment changes rapidly and predictably along an elevation gradient, and such variation may be expected to lead to the evolution of local adaptations. In food-caching mountain chickadees, Poecile gambeli, reliance on food stores is likely to increase with elevation, and previous research has shown that individuals living at high elevations cache more food and have superior spatial memory, needed to recover food caches, while also being socially subordinate to low-elevation birds. Here, we asked whether such differences might be associated with assortative mating. Considering that superior spatial memory ability for recovering food caches may be more critical for survival at high elevations because of more severe winter conditions, it should benefit females from high elevations to mate assortatively with males from the same elevation. If spatial memory is costly but not critical at low elevations, females from low elevation should mate assortatively with males from low elevation, especially given their socially dominant status to high-elevation birds. We assessed female preference using a pairwise choice of high- and low-elevation males. We used the amount of time spent in proximity to males from the same versus different elevation to determine female preference. High-elevation females showed significant preference for high-elevation males, however, low-elevation females showed no elevation-related preference. These results suggest that high-elevation females are choosier than low-elevation females, and prefer males from their same elevation.

Elevation-related differences in novel environment exploration and social dominance in food-caching mountain chickadees

Harsh and unpredictable environments have been assumed to favor the evolution of better learning abilities in animals. At the same time, individual variation in learning abilities might be associated with variation in other correlated traits potentially forming a behavioral syndrome. We have previously reported significant elevation-related differences in spatial memory and the hippocampus in food-caching mountain chickadees. Here, we tested for elevation-related differences in novel environment exploration, neophobia, and social dominance—behavioral traits previously thought to correlate with individual variation in cognition, using different birds from the same elevations. Compared to low-elevation birds, high-elevation chickadees were slower at novel environment exploration, but there were no detectable differences in neophobia. High-elevation chickadees were also socially subordinate to low-elevation chickadees in pairwise interactions. Considering previously reported elevation-related differences in cognition and the brain, our results suggest, however indirectly, that elevation-related variation in spatial memory might be associated with differences in novel environment exploration and in ability to obtain a high social rank in winter social groups. Whether these behavioral traits represent a behavioral syndrome or whether climate might affect these traits independently, our results suggest that multiple differences between elevations might assist with elevation-related separation. High-elevation chickadees would likely experience higher mortality if they move to lower elevation due to their low social dominance status and low-elevation chickadees might experience higher mortality if they move to higher elevation due to reduced memory ability and lack of behavioral adaptations to colder climate.

Untangling Elevation-Related Differences in the Hippocampus in Food-Caching Mountain Chickadees: The Effect of a Uniform Captive Environment

Variation in environmental conditions associated with differential selection on spatial memory has been hypothesized to result in evolutionary changes in the morphology of the hippocampus, a brain region involved in spatial memory. At the same time, it is well known that the morphology of the hippocampus might also be directly affected by environmental conditions. Understanding the role of environment-based plasticity is therefore critical when investigating potential adaptive evolutionary changes in the hippocampus associated with environmental variation. We previously demonstrated large elevation-related variation in hippocampus morphology in mountain chickadees over an extremely small spatial scale. We hypothesized that this variation is related to differential selection pressures associated with differences in winter climate severity along an elevation gradient, which make different demands on spatial memory used for food cache retrieval. Here, we tested whether such variation is experience based, generated by potential differences in the environment, by comparing the hippocampus morphology of chickadees from different elevations maintained in a uniform captive environment in a laboratory with those sampled directly from the wild. In addition, we compared hippocampal neuron soma size in chickadees sampled directly from the wild with those maintained in laboratory conditions with restricted and unrestricted spatial memory use via manipulation of food-caching experiences to test whether memory use can affect neuron soma size. There were significant elevation-related differences in hippocampus volume and the total number of hippocampal neurons, but not in neuron soma size, in captive birds. Captive environmental conditions were associated with a large reduction in hippocampus volume and neuron soma size, but not in the total number of neurons or in neuron soma size in other telencephalic regions. Restriction of memory use while in laboratory conditions produced no significant effects on hippocampal neuron soma size. Overall our results showed that captivity has a strong effect on hippocampus volume, which could be due, at least partly, to a reduction in neuron soma size specifically in the hippocampus, but it did not override elevation-related differences in hippocampus volume or in the total number of hippocampal neurons. These data are consistent with the idea of the adaptive nature of the elevation-related differences associated with selection on spatial memory, while at the same time demonstrating additional environment-based plasticity in hippocampus volume, but not in neuron numbers. Our results, however, cannot rule out that the differences between elevations might still be driven by some developmental or early posthatching conditions/experiences.