Dovid Y. Kozlovsky

Problem-solving ability and response to novelty in mountain chickadees (Poecile gambeli) from different elevations

Animals inhabiting challenging and harsh environments are expected to benefit from certain phenotypic traits including cognitive abilities. In particular, innovation and habituation are traits thought to benefit animals in challenging environments and increase individual’s probability of survival via increased foraging success. Here, we tested whether mountain chickadees from two elevations varying in winter climate severity differed in two traits involving innovation and habituation–problem-solving ability and response to novelty. Higher montane elevations are associated with a significantly longer winter period characterized by lower temperatures and more snow, making winter survival more challenging due to a probable increase in foraging demands. Mountain chickadees inhabiting the harsher high elevation were significantly faster at solving a novel problem than their low elevation counterparts. Birds from both elevations responded with increased latency to approach the novel object; however, there were no elevation-related differences. Male and female chickadees responded similarly on both tasks, suggesting no sex-related differences in problem solving ability or neophobia. The problem solving results are consistent with the results for closely related black-capped chickadees along a longitudinal gradient of winter climatic harshness on a larger geographic scale, but the response to novelty data is not. Overall, our data support the hypothesis that enhanced problem solving ability might be associated with living in harsher environments either via natural selection or by plastic response to different environments and suggest that differences in problem solving ability do not have to be associated with differences in neophobia.

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.

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.

Elevation related variation in aggressive response to mirror image in mountain chickadees

Behavioural syndrome literature suggests that behavioural traits may be coupled to form behavioural strategies that are consistent and repeatable across contexts. Typically these behavioural types are composed of bold, aggressive, dominant individuals and shy, less aggressive, subordinate individuals. Mountain chickadees living in varying climatic conditions across a montane environment appear to exhibit consistent behavioural types, such that high elevation birds, which experience harsher winter conditions and rely more heavily on spatial memory to retrieve food caches to survive winter, explore a novel environment at a slower rate (i.e., shy) and are socially subordinate to low elevation birds. Dominance is typically expressed in individual pairwise interactions, but it is not always clear which traits predispose an individual to become a dominant in such interactions. Aggression is frequently suggested to be associated with higher dominance status, yet the data are equivocal. Here we aimed to test whether previously described elevation related differences in social dominance might be associated with elevation related differences in aggression levels in mountain chickadees by using the mirror test. The mirror test can address potential differences in reactive and proactive aggression, although caution should be taken when using the mirror test as some species are able to self-recognize. Low elevation birds responded more aggressively to their mirror image than high elevation birds, suggesting that elevation related differences in aggression may be partially responsible for previously found differences in social dominance status.

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.

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.

Chickadees with Bigger Brains Have Smaller Digestive Tracts: A Multipopulation Comparison

The factors leading to the evolution of large brain size remain controversial. Brains are metabolically expensive and larger brains demand higher maintenance costs. The expensive-tissue hypothesis suggests that when selection favors larger brains, evolutionary changes in brain size can occur without an overall increase in energetic costs when brain size represents a trade-off with the size of other expensive tissues, such as the digestive tract. Still, support for this hypothesis is equivocal. We compared mean brain mass, digestive tract mass (stomach and gut) and heart mass in 9 populations of black-capped chickadees along a gradient of winter climate severity. Mean brain mass and telencephalon volume showed significant population variation with larger brains associated with harsher winter conditions. Mean population brain mass and telencephalon volume were also negatively related to both stomach and gut mass. Mean population heart mass, on the other hand, was not significantly associated with either mean brain mass or winter climate severity. Mean brain mass was negatively associated with body mass, with chickadees from harsher environments being smaller but having larger brains and smaller digestive tracts. Our results are consistent with the expensive-tissue hypothesis, and suggest that a harsher winter climate might favor larger brains, which might be associated with a reduction in size of the digestive tract. These findings could potentially be a result of population differences in the winter climate diet related to the perishability of more efficient invertebrate-based food caches.

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, Neis 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.

Fluctuations in annual climatic extremes are associated with reproductive variation in resident mountain chickadees

Mounting evidence suggests that we are experiencing rapidly accelerating global climate change. Understanding how climate change may affect life is critical to identifying species and populations that are vulnerable. Most current research focuses on investigating how organisms may respond to gradual warming, but another effect of climate change is extreme annual variation in precipitation associated with alternations between drought and unusually heavy precipitation, like that exhibited in the western regions of North America. Understanding climate change effects on animal reproductive behaviour is especially important, because it directly impacts population persistence. Here, we present data on reproduction in nest-box breeding, resident mountain chickadees inhabiting high and low elevations in the Sierra Nevada across 5 years. These 5 years of data represent the full range of climatic variation from the largest drought in five centuries to one of the heaviest snow years on record. There were significant differences in most reproductive characteristics associated with variation in climate. Both climate extremes were negatively associated with reproductive success at high and low elevations, but low-elevation chickadees had worse reproductive success in the largest drought year while high-elevation chickadees had worse reproductive success in the heaviest snow year. Considering that the frequency of extreme climate swings between drought and snow is predicted to increase, such swings may have negative effects on chickadee populations across the entire elevation gradient, as climatic extremes should favour different adaptations. Alternatively, it is possible that climate fluctuations might favour preserving genetic variation allowing for higher resilience. It is too early to make specific predictions regarding how increased frequency of extreme climate fluctuation may impact chickadees; however, our data suggest that even the most common species may be susceptible.

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.