Fecal DNA metabarcoding helps characterize the Canada jay's diet and confirms its reliance on stored food for winter survival and breeding.

Accurately determining the diet of wild animals can be challenging if food items are small, visible only briefly, or rendered visually unidentifiable in the digestive system. In some food caching species, an additional challenge is determining whether consumed diet items have been previously stored or are fresh. The Canada jay (Perisoreus canadensis) is a generalist resident of North American boreal and subalpine forests with anatomical and behavioural adaptations allowing it to make thousands of arboreal food caches in summer and fall that are presumably responsible for its high winter survival and late winter/early spring breeding. We used DNA fecal metabarcoding to obtain novel information on nestling diets and compiled a dataset of 662 published and unpublished direct observations or stomach contents identifications of natural foods consumed by Canada jays throughout the year. We then used detailed natural history information to make informed decisions on whether each item identified to species in the diets of winter adults and nestlings was best characterized as 'likely cached', 'likely fresh' (i.e., was available as a non-cached item when it appeared in a jay's feces or stomach), or 'either possible'. Of the 87 food items consumed by adults in the winter, 39% were classified as 'likely cached' and 6% were deemed to be 'likely fresh'. For nestlings, 29% of 125 food items identified to species were 'likely cached' and 38% were 'likely fresh'. Our results support both the indispensability of cached food for Canada jay winter survival and previous suggestions that cached food is important for late winter/early spring breeding. Our work highlights the value of combining metabarcoding, stomach contents analysis, and direct observations to determine the cached vs. non-cached origins of consumed food items and the identity of food caches, some of which could be especially vulnerable to degradation through climate change.

Early-life sibling conflict in Canada jays has lifetime fitness consequences.

While delaying natal dispersal can provide short-term benefits for juveniles, lifetime fitness consequences are rarely assessed. Furthermore, competition for limited positions on a natal territory could impose an indirect fitness cost on the winner if the outcome has negative effects on its siblings. We use radio-tracking and 58 years of nesting data in Ontario, Canada to examine the lifetime fitness consequences of sibling expulsion in the Canada jay (Perisoreus canadensis). Six weeks after fledging, intra-brood dominance struggles result in one 'dominant juvenile' (DJ) remaining on the natal territory after expelling its subordinate siblings, the 'ejectees' (EJs). Despite an older age-at-first-reproduction, DJs produced more recruits over their lifetime and had higher first-year survival than EJs, leading to substantially higher direct fitness. Even though DJs incurred an indirect fitness cost by expelling their siblings and there was no evidence that their presence on the natal territory increased their parents' reproductive output the following year, they still had substantially higher inclusive fitness than EJs. Our results demonstrate how early-life sibling conflict can have lifetime consequences and that such fitness differences in Canada jays are driven by the enhanced first-year survival of DJs pursuant to the early-summer expulsion of their sibling competitors.

Early-life experience shapes patterns of senescence in a food-caching passerine.

For many species, breeding performance increases through early adulthood followed by declines later in life. Although patterns of age-specific decline have been shown to vary between individuals, the factors that lead to this individual variation in the intensity of reproductive senescence are yet to be fully understood. We investigated whether early-life social status influenced age-related trends in the breeding performance of male Canada jays (Perisoreus canadensis), year-round residents of North America's boreal and sub-alpine forests. Shortly after young become nutritionally independent, intra-brood dominance struggles lead to one juvenile (Dominant Juvenile) remaining on the natal territory after expelling its subordinate siblings (Ejectees). First, we show via radio tracking that in our declining range-edge population Ejectees either join an unrelated pair (67%), form a breeding pair with another bird (28%) or occupy a territory alone (5%). Second, using 39 years of breeding data, we demonstrate that Ejectee males advanced laying dates and increased the annual number of nestlings until 6 years of age before declining, whereas Dominant Juvenile males advanced laying dates until 11 years and increased annual number of nestlings until 12 years of age before declining. This study documents clear variation in ageing patterns between dominant and expelled young, with implications for the role of early-life experiences and phenotypic quality in determining patterns of ageing.

Early-Life Corticosterone Body Condition Influence Social Status and Survival in a Food-Caching Passerine.

Individuals undergo profound changes throughout their early life as they grow and transition between life-history stages. As a result, the conditions that individuals experience during development can have both immediate and lasting effects on their physiology, behavior, and, ultimately, fitness. In a population of Canada jays in Algonquin Provincial Park, Ontario, Canada, we characterized the diet composition and physiological profile of young jays at three key time points during development (nestling, pre-fledge, and pre-dispersal) by quantifying stable-carbon (δ13C) and -nitrogen (δ15N) isotopes and corticosterone concentrations in feathers. We then investigated the downstream effects of early-life diet composition, feather corticosterone, and environmental conditions on a juvenile's social status, body condition, and probability of being observed in the fall following hatch. Across the three time points, the diet of Canada jay young was composed primarily of vertebrate tissue and human food with the proportion of these food items increasing as the jays neared dispersal. Feather corticosterone concentrations also shifted across the three time points, decreasing from nestling to pre-dispersal. Dominant juveniles had elevated corticosterone concentrations in their feathers grown pre-dispersal compared with subordinates. High body condition as nestlings was associated with high body condition as juveniles and an increased probability of being observed in the fall. Together, our results demonstrate that nestling physiology and body condition influence the social status and body condition once individuals are independent, with potential long-term consequences on survival and fitness.

Environmental conditions modulate compensatory effects of site dependence in a food-caching passerine.

Although density regulates the abundance of most wild animal populations by influencing vital rates, such as fecundity and survival, the mechanisms responsible for generating negative density dependence are unclear for many species. Site dependence occurs when there is preferential filling of high-quality territories, which results in higher per capita vital rates at low densities because a larger proportion of occupied territories are of high quality. Using 41 yr of territory occupancy and demographic data, we investigated whether site dependence was a mechanism acting to influence fecundity and, by extension, regulate a population of Canada Jays in Algonquin Provincial Park, Ontario, Canada. As predicted by site dependence, the proportion of occupied territories that were of high quality was negatively correlated with population density and periods of vacancy were shorter for high-quality territories than for low-quality territories. We also found evidence that per capita fecundity was positively related to the proportion of occupied territories that were of high quality, but only when environmental conditions, which influence the entire population, were otherwise poor for breeding. Our results suggest that site dependence likely plays a role in regulating this population but that environmental conditions can modulate the strength of density dependence.

Climate-driven carry-over effects negatively influence population growth rate in a food-caching boreal passerine.

Understanding how events throughout the annual cycle are linked is important for predicting variation in individual fitness, but whether and how carry-over effects scale up to influence population dynamics is poorly understood. Using 38 years of demographic data from Algonquin Provincial Park, Ontario, and a full annual cycle integrated population model, we examined the influence of environmental conditions and density on the population growth rate of Canada jays (Perisoreus canadensis), a resident boreal passerine that relies on perishable cached food for over-winter survival and late-winter breeding. Our results demonstrate that fall environmental variables, most notably the number of freeze-thaw events, carried over to influence late-winter fecundity, which, in turn, was the main vital rate driving population growth. These results are consistent with the hypothesis that warmer and more variable fall conditions accelerate the degradation of perishable stored food that is relied upon for successful reproduction. Future warming during the fall and winter may compromise the viability of cached food that requires consistent subzero temperatures for effective preservation, potentially exacerbating climate-driven carry-over effects that impact long-term population dynamics.

Autumn freeze-thaw events carry over to depress late-winter reproductive performance in Canada jays.

Evidence suggests that range-edge populations are highly vulnerable to the impacts of climate change, but few studies have examined the specific mechanisms that are driving observed declines. Species that store perishable food for extended periods of time may be particularly susceptible to environmental change because shifts in climatic conditions could accelerate the natural degradation of their cached food. Here, we use 40 years of breeding data from a marked population of Canada jays (Perisoreus canadensis) located at the southern edge of their range in Algonquin Provincial Park, Ontario, to examine whether climatic conditions prior to breeding carry over to influence reproductive performance. We found that multiple measures of Canada jay reproductive performance (brood size, nest success and nestling condition) in the late winter were negatively correlated with the number of freeze-thaw events the previous autumn. Our results suggest that freeze-thaw events have a significant detrimental impact on the quality and/or quantity of cached food available to Canada jays. Future increases in such events, caused by climate change, could pose a serious threat to Canada jays and other food caching species that store perishable foods for long periods of time.

Reduced reproductive performance associated with warmer ambient temperatures during incubation in a winter-breeding, food-storing passerine.

Timing of reproduction can influence individual fitness whereby early breeders tend to have higher reproductive success than late breeders. However, the fitness consequences of timing of breeding may also be influenced by environmental conditions after the commencement of breeding. We tested whether ambient temperatures during the incubation and early nestling periods modulated the effect of laying date on brood size and dominant juvenile survival in gray jays (Perisoreus canadensis), a sedentary boreal species whose late winter nesting depends, in part, on caches of perishable food. Previous evidence has suggested that warmer temperatures degrade the quality of these food hoards, and we asked whether warmer ambient temperatures during the incubation and early nestling periods would be associated with smaller brood sizes and lower summer survival of dominant juveniles. We used 38 years of data from a range-edge population of gray jays in Algonquin Provincial Park, Ontario, where the population has declined over 50% since the study began. Consistent with the "hoard-rot" hypothesis, we found that cold temperatures during incubation were associated with larger brood sizes in later breeding attempts, but temperatures had little effect on brood size for females breeding early in the season. This is the first evidence that laying date and temperature during incubation interactively influence brood size in any bird species. We did not find evidence that ambient temperatures during the incubation period or early part of the nestling period influenced summer survival of dominant juveniles. Our findings provide evidence that warming temperatures are associated with some aspects of reduced reproductive performance in a species that is reliant on cold temperatures to store perishable food caches, some of which are later consumed during the reproductive period.

An example of phenotypic adherence to the island rule? - Anticosti gray jays are heavier but not structurally larger than mainland conspecifics.

The island rule refers to the tendency of small vertebrates to become larger when isolated on islands and the frequent dwarfing of large forms. It implies genetic control, and a necessary linkage, of size and body-mass differences between insular and mainland populations. To examine the island rule, we compared body size and mass of gray jays (Perisoreus canadensis) on Anticosti Island, Québec, located in the Gulf of St. Lawrence, with three mainland populations (2 in Québec and 1 in Ontario). Although gray jays on Anticosti Island were ca 10% heavier, they were not structurally larger, than the three mainland populations. This suggests that Anticosti jays are not necessarily genetically distinct from mainland gray jays and that they may have achieved their greater body masses solely through packing more mass onto mainland-sized body frames. As such, they may be the first-known example of a proposed, purely phenotypic initial step in the adherence to the island rule by an insular population. Greater jay body mass is probably advantageous in Anticosti's high-density, intensely competitive social environment that may have resulted from the island's lack of mammalian nest predators.

Experimental evidence and 43 years of monitoring data show that food limits reproduction in a food-caching passerine.

Several species of birds and mammals overcome periods of scarcity by caching food, but for the vast majority of species, it is virtually unknown whether they are food limited during these periods. The Gray Jay (Perisoreus canadensis) is a boreal-resident, food-caching passerine that breeds in late winter when fresh food is scarce. Using a two-year experiment and 43 years of monitoring data, we examined the food limitation hypothesis in a population of Gray Jays in Algonquin Park, Ontario, Canada, that has declined by over 50% in the last three decades. Breeding pairs that were experimentally food supplemented during the pre-breeding period laid eggs earlier in the season and had larger brood sizes than non-supplemented controls. From the long-term data, we found strong evidence that pairs that were regularly supplemented by the public (park visitors) tended to lay eggs earlier and have larger clutches and brood sizes compared to pairs that were not supplemented. Nestling body condition (mass controlled for body size) was not influenced by either experimental or public food supplementation. Our results support the hypothesis that Gray Jays are food limited during their late-winter breeding period and suggest that warmer fall temperatures, which have been hypothesized to lead to cache spoilage, may have a significant impact on reproductive success in this declining population. Moreover, our results contribute to understanding how public feeding can influence the fitness of wild animals.

Contrasting patterns of survival and dispersal in multiple habitats reveal an ecological trap in a food-caching bird.

A comprehensive understanding of how natural and anthropogenic variation in habitat influences populations requires long-term information on how such variation affects survival and dispersal throughout the annual cycle. Gray jays Perisoreus canadensis are widespread boreal resident passerines that use cached food to survive over the winter and to begin breeding during the late winter. Using multistate capture-recapture analysis, we examined apparent survival and dispersal in relation to habitat quality in a gray jay population over 34 years (1977-2010). Prior evidence suggests that natural variation in habitat quality is driven by the proportion of conifers on territories because of their superior ability to preserve cached food. Although neither adults (>1 year) nor juveniles (<1 year) had higher survival rates on high-conifer territories, both age classes were less likely to leave high-conifer territories and, when they did move, were more likely to disperse to high-conifer territories. In contrast, survival rates were lower on territories that were adjacent to a major highway compared to territories that did not border the highway but there was no evidence for directional dispersal towards or away from highway territories. Our results support the notion that natural variation in habitat quality is driven by the proportion of coniferous trees on territories and provide the first evidence that high-mortality highway habitats can act as an equal-preference ecological trap for birds. Reproductive success, as shown in a previous study, but not survival, is sensitive to natural variation in habitat quality, suggesting that gray jays, despite living in harsh winter conditions, likely favor the allocation of limited resources towards self-maintenance over reproduction.

Experimental evidence for a novel mechanism driving variation in habitat quality in a food-caching bird.

Variation in habitat quality can have important consequences for fitness and population dynamics. For food-caching species, a critical determinant of habitat quality is normally the density of storable food, but it is also possible that quality is driven by the ability of habitats to preserve food items. The food-caching gray jay (Perisoreus canadensis) occupies year-round territories in the coniferous boreal and subalpine forests of North America, but does not use conifer seed crops as a source of food. Over the last 33 years, we found that the occupancy rate of territories in Algonquin Park (ON, Canada) has declined at a higher rate in territories with a lower proportion of conifers compared to those with a higher proportion. Individuals occupying territories with a low proportion of conifers were also less likely to successfully fledge young. Using chambers to simulate food caches, we conducted an experiment to examine the hypothesis that coniferous trees are better able to preserve the perishable food items stored in summer and fall than deciduous trees due to their antibacterial and antifungal properties. Over a 1-4 month exposure period, we found that mealworms, blueberries, and raisins all lost less weight when stored on spruce and pine trees compared to deciduous and other coniferous trees. Our results indicate a novel mechanism to explain how habitat quality may influence the fitness and population dynamics of food-caching animals, and has important implications for understanding range limits for boreal breeding animals.

Climate change and the demographic demise of a hoarding bird living on the edge.

Population declines along the lower-latitude edge of a species' range may be diagnostic of climate change. We report evidence that climate change has contributed to deteriorating reproductive success in a rapidly declining population of the grey jay (Perisoreus canadensis) at the southern edge of its range. This non-migratory bird of boreal and subalpine forest lives on permanent territories, where it hoards enormous amounts of food for winter and then breeds very early, under still-wintry conditions. We hypothesized that warmer autumns have increased the perishability of hoards and compromised subsequent breeding attempts. Our analysis confirmed that warm autumns, especially when followed by cold late winters, have led to delayed breeding and reduced reproductive success. Our findings uniquely show that weather months before the breeding season impact the timing and success of breeding. Warm autumns apparently represent hostile conditions for this species, because it relies on cold storage. Our study population may be especially vulnerable, because it is situated at the southern edge of the range, where the potential for hoard rot is most pronounced. This population's demise may signal a climate-driven range contraction through local extinctions along the trailing edge.