A hard fruit to swallow.

Foraging niches become more specialized toward bird range limits.

An arctic breeding songbird overheats during intense activity even at low air temperatures.

Birds maintain some of the highest body temperatures among endothermic animals. Often deemed a selective advantage for heat tolerance, high body temperatures also limits birds' thermal safety margin before reaching lethal levels. Recent modelling suggests that sustained effort in Arctic birds might be restricted at mild air temperatures, which may require reductions in activity to avoid overheating, with expected negative impacts on reproductive performance. We measured within-individual changes in body temperature in calm birds and then in response to an experimental increase in activity in an outdoor captive population of Arctic, cold-specialised snow buntings (Plectrophenax nivalis), exposed to naturally varying air temperatures (- 15 to 36 °C). Calm buntings exhibited a modal body temperature range from 39.9 to 42.6 °C. However, we detected a significant increase in body temperature within minutes of shifting calm birds to active flight, with strong evidence for a positive effect of air temperature on body temperature (slope = 0.04 °C/ °C). Importantly, by an ambient temperature of 9 °C, flying buntings were already generating body temperatures ≥ 45 °C, approaching the upper thermal limits of organismal performance (45-47 °C). With known limited evaporative heat dissipation capacities in these birds, our results support the recent prediction that free-living buntings operating at maximal sustainable rates will increasingly need to rely on behavioural thermoregulatory strategies to regulate body temperature, to the detriment of nestling growth and survival.

Temperate species underfill their tropical thermal potentials on land.

Understanding how temperature determines the distribution of life is necessary to assess species' sensitivities to contemporary climate change. Here, we test the importance of temperature in limiting the geographic ranges of ectotherms by comparing the temperatures and areas that species occupy to the temperatures and areas species could potentially occupy on the basis of their physiological thermal tolerances. We find that marine species across all latitudes and terrestrial species from the tropics occupy temperatures that closely match their thermal tolerances. However, terrestrial species from temperate and polar latitudes are absent from warm, thermally tolerable areas that they could potentially occupy beyond their equatorward range limits, indicating that extreme temperature is often not the factor limiting their distributions at lower latitudes. This matches predictions from the hypothesis that adaptation to cold environments that facilitates survival in temperate and polar regions is associated with a performance trade-off that reduces species' abilities to contend in the tropics, possibly due to biotic exclusion. Our findings predict more direct responses to climate warming of marine ranges and cool range edges of terrestrial species.

Mapping nationally and globally at-risk species to identify hotspots for (and gaps in) conservation.

Protecting habitat of species at risk is critical to their recovery, but can be contentious. For example, protecting species that are locally imperilled but globally common is often thought to distract from protecting globally imperilled species. However, such perceived trade-offs are based on the assumption that threatened groups have little spatial overlap, which is rarely quantified. We compiled range maps of terrestrial species at risk in Canada to assess the geographic overlap of nationally and globally at-risk species with each other, among taxonomic groups, and with protected areas. While many nationally at-risk taxa only occur in Canada at their northern range edge, they are not significantly more peripheral in Canada than globally at-risk species. Further, 56% of hotspots of nationally at-risk taxa are also hotspots of globally at-risk species, undercutting the perceived trade-off in their protection. While strong spatial overlap across threat levels and taxa should facilitate efficient habitat protection, less than 7% of the area in Canada's at-risk hotspots is protected, and two-thirds of nationally and globally at-risk species in Canada have less than 10% of their Canadian range protected. Our results counter the perception that protecting nationally versus globally at-risk species are at odds, and identify critical areas to target as Canada strives to increase its protected areas and promote recovery of species at risk.

Rapid upwards spread of non-native plants in mountains across continents.

High-elevation ecosystems are among the few ecosystems worldwide that are not yet heavily invaded by non-native plants. This is expected to change as species expand their range limits upwards to fill their climatic niches and respond to ongoing anthropogenic disturbances. Yet, whether and how quickly these changes are happening has only been assessed in a few isolated cases. Starting in 2007, we conducted repeated surveys of non-native plant distributions along mountain roads in 11 regions from 5 continents. We show that over a 5- to 10-year period, the number of non-native species increased on average by approximately 16% per decade across regions. The direction and magnitude of upper range limit shifts depended on elevation across all regions. Supported by a null-model approach accounting for range changes expected by chance alone, we found greater than expected upward shifts at lower/mid elevations in at least seven regions. After accounting for elevation dependence, significant average upward shifts were detected in a further three regions (revealing evidence for upward shifts in 10 of 11 regions). Together, our results show that mountain environments are becoming increasingly exposed to biological invasions, emphasizing the need to monitor and prevent potential biosecurity issues emerging in high-elevation ecosystems.

Warming in the land of the midnight sun: breeding birds may suffer greater heat stress at high- versus low-Arctic sites.

Rising global temperatures are expected to increase reproductive costs for wildlife as greater thermoregulatory demands interfere with reproductive activities. However, predicting the temperatures at which reproductive performance is negatively impacted remains a significant hurdle. Using a thermoregulatory polygon approach, we derived a reproductive threshold temperature for an Arctic songbird-the snow bunting (Plectrophenax nivalis). We defined this threshold as the temperature at which individuals must reduce activity to suboptimal levels (i.e. less than four-time basal metabolic rate) to sustain nestling provisioning and avoid overheating. We then compared this threshold to operative temperatures recorded at high (82° N) and low (64° N) Arctic sites to estimate how heat constraints translate into site-specific impacts on sustained activity level. We predict buntings would become behaviourally constrained at operative temperatures above 11.7°C, whereupon they must reduce provisioning rates to avoid overheating. Low-Arctic sites had larger fluctuations in solar radiation, consistently producing daily periods when operative temperatures exceeded 11.7°C. However, high-latitude birds faced entire, consecutive days when parents would be unable to sustain required provisioning rates. These data indicate that Arctic warming is probably already disrupting the breeding performance of cold-specialist birds and suggests counterintuitive and severe negative impacts of warming at higher latitude breeding locations.

Effects of species interactions on the potential for evolution at species' range limits.

Species' ranges are limited by both ecological and evolutionary constraints. While there is a growing appreciation that ecological constraints include interactions among species, like competition, we know relatively little about how interactions contribute to evolutionary constraints at species' niche and range limits. Building on concepts from community ecology and evolutionary biology, we review how biotic interactions can influence adaptation at range limits by impeding the demographic conditions that facilitate evolution (which we term a 'demographic pathway to adaptation'), and/or by imposing evolutionary trade-offs with the abiotic environment (a 'trade-offs pathway'). While theory for the former is well-developed, theory for the trade-offs pathway is not, and empirical evidence is scarce for both. Therefore, we develop a model to illustrate how fitness trade-offs along biotic and abiotic gradients could affect the potential for range expansion and niche evolution following ecological release. The model shows that which genotypes are favoured at species' range edges can depend strongly on the biotic context and the nature of fitness trade-offs. Experiments that characterize trade-offs and properly account for biotic context are needed to predict which species will expand their niche or range in response to environmental change. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Think globally, measure locally: The MIREN standardized protocol for monitoring plant species distributions along elevation gradients.

Climate change and other global change drivers threaten plant diversity in mountains worldwide. A widely documented response to such environmental modifications is for plant species to change their elevational ranges. Range shifts are often idiosyncratic and difficult to generalize, partly due to variation in sampling methods. There is thus a need for a standardized monitoring strategy that can be applied across mountain regions to assess distribution changes and community turnover of native and non-native plant species over space and time. Here, we present a conceptually intuitive and standardized protocol developed by the Mountain Invasion Research Network (MIREN) to systematically quantify global patterns of native and non-native species distributions along elevation gradients and shifts arising from interactive effects of climate change and human disturbance. Usually repeated every five years, surveys consist of 20 sample sites located at equal elevation increments along three replicate roads per sampling region. At each site, three plots extend from the side of a mountain road into surrounding natural vegetation. The protocol has been successfully used in 18 regions worldwide from 2007 to present. Analyses of one point in time already generated some salient results, and revealed region-specific elevational patterns of native plant species richness, but a globally consistent elevational decline in non-native species richness. Non-native plants were also more abundant directly adjacent to road edges, suggesting that disturbed roadsides serve as a vector for invasions into mountains. From the upcoming analyses of time series, even more exciting results can be expected, especially about range shifts. Implementing the protocol in more mountain regions globally would help to generate a more complete picture of how global change alters species distributions. This would inform conservation policy in mountain ecosystems, where some conservation policies remain poorly implemented.

Does pollen limitation limit plant ranges? Evidence and implications.

Sexual reproduction often declines towards range edges, reducing fitness, dispersal and adaptive potential. For plants, sexual reproduction is frequently limited by inadequate pollination. While case studies show that pollen limitation can limit plant distributions, the extent to which pollination commonly declines towards plant range edges is unknown. Here, we use global databases of pollen-supplementation experiments and plant occurrence data to test whether pollen limitation increases towards plant range edges, using a phylogenetically controlled meta-analysis. While there was significant pollen limitation across studies, we found little evidence that pollen limitation increases towards plant range edges. Pollen limitation was not stronger towards the tropics, nor at species' equatorward versus poleward range limits. Meta-analysis results are consistent with results from targeted experiments, in which pollen limitation increased significantly towards only 14% of 14 plant range edges, suggesting that pollination contributes to range limits less often than do other interactions. Together, these results suggest pollination is one of the rich variety of potential ecological factors that can contribute to range limits, rather than a generally important constraint on plant distributions. This article is part of the theme issue 'Species' ranges in the face of changing environments (part I)'.

Biotic interactions are more often important at species' warm versus cool range edges.

Predicting which ecological factors constrain species distributions is a fundamental ecological question and critical to forecasting geographic responses to global change. Darwin hypothesised that abiotic factors generally impose species' high-latitude and high-elevation (typically cool) range limits, whereas biotic interactions more often impose species' low-latitude/low-elevation (typically warm) limits, but empirical support has been mixed. Here, we clarify three predictions arising from Darwin's hypothesis and show that previously mixed support is partially due to researchers testing different predictions. Using a comprehensive literature review (885 range limits), we find that biotic interactions, including competition, predation and parasitism, contributed to >60% of range limits and influenced species' warm limits more often than cool limits. Abiotic factors contributed more often than biotic interactions to cool range limits, but temperature contributed frequently to both cool and warm limits. Our results suggest that most range limits will be sensitive to climate warming, but warm-limit responses in particular will depend strongly on biotic interactions.

Limited heat tolerance in a cold-adapted seabird: implications of a warming Arctic.

The Arctic is warming at approximately twice the global rate, with well-documented indirect effects on wildlife. However, few studies have examined the direct effects of warming temperatures on Arctic wildlife, leaving the importance of heat stress unclear. Here, we assessed the direct effects of increasing air temperatures on the physiology of thick-billed murres (Uria lomvia), an Arctic seabird with reported mortalities due to heat stress while nesting on sun-exposed cliffs. We used flow-through respirometry to measure the response of body temperature, resting metabolic rate, evaporative water loss and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production) in murres while experimentally increasing air temperature. Murres had limited heat tolerance, exhibiting: (1) a low maximum body temperature (43.3°C); (2) a moderate increase in resting metabolic rate relative that within their thermoneutral zone (1.57 times); (3) a small increase in evaporative water loss rate relative that within their thermoneutral zone (1.26 times); and (4) a low maximum evaporative cooling efficiency (0.33). Moreover, evaporative cooling efficiency decreased with increasing air temperature, suggesting murres were producing heat at a faster rate than they were dissipating it. Larger murres also had a higher rate of increase in resting metabolic rate and a lower rate of increase in evaporative water loss than smaller murres; therefore, evaporative cooling efficiency declined with increasing body mass. As a cold-adapted bird, murres' limited heat tolerance likely explains their mortality on warm days. Direct effects of overheating on Arctic wildlife may be an important but under-reported impact of climate change.

Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion.

Every species experiences limits to its geographic distribution. Some evolutionary models predict that populations at range edges are less well adapted to their local environments due to drift, expansion load, or swamping gene flow from the range interior. Alternatively, populations near range edges might be uniquely adapted to marginal environments. In this study, we use a database of transplant studies that quantify performance at broad geographic scales to test how local adaptation, site quality, and population quality change from spatial and climatic range centers toward edges. We find that populations from poleward edges perform relatively poorly, both on average across all sites (15% lower population quality) and when compared to other populations at home (31% relative fitness disadvantage), consistent with these populations harboring high genetic load. Populations from equatorial edges also perform poorly on average (18% lower population quality) but, in contrast, outperform foreign populations (16% relative fitness advantage), suggesting that populations from equatorial edges have strongly adapted to unique environments. Finally, we find that populations from sites that are thermally extreme relative to the species' niche demonstrate strong local adaptation, regardless of their geographic position. Our findings indicate that both nonadaptive processes and adaptive evolution contribute to variation in adaptation across species' ranges.

Limited heat tolerance in an Arctic passerine: Thermoregulatory implications for cold-specialized birds in a rapidly warming world.

Arctic animals inhabit some of the coldest environments on the planet and have evolved physiological mechanisms for minimizing heat loss under extreme cold. However, the Arctic is warming faster than the global average and how well Arctic animals tolerate even moderately high air temperatures (T a) is unknown.Using flow-through respirometry, we investigated the heat tolerance and evaporative cooling capacity of snow buntings (Plectrophenax nivalis; ≈31 g, N = 42), a cold specialist, Arctic songbird. We exposed buntings to increasing T a and measured body temperature (T b), resting metabolic rate (RMR), rates of evaporative water loss (EWL), and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production).Buntings had an average (±SD) T b of 41.3 ± 0.2°C at thermoneutral T a and increased T b to a maximum of 43.5 ± 0.3°C. Buntings started panting at T a of 33.2 ± 1.7°C, with rapid increases in EWL starting at T a = 34.6°C, meaning they experienced heat stress when air temperatures were well below their body temperature. Maximum rates of EWL were only 2.9× baseline rates at thermoneutral T a, a markedly lower increase than seen in more heat-tolerant arid-zone species (e.g., ≥4.7× baseline rates). Heat-stressed buntings also had low evaporative cooling efficiencies, with 95% of individuals unable to evaporatively dissipate an amount of heat equivalent to their own metabolic heat production.Our results suggest that buntings' well-developed cold tolerance may come at the cost of reduced heat tolerance. As the Arctic warms, and this and other species experience increased periods of heat stress, a limited capacity for evaporative cooling may force birds to increasingly rely on behavioral thermoregulation, such as minimizing activity, at the expense of diminished performance or reproductive investment.

Clustered versus catastrophic global vertebrate declines.

Recent analyses have reported catastrophic global declines in vertebrate populations1,2. However, the distillation of many trends into a global mean index obscures the variation that can inform conservation measures and can be sensitive to analytical decisions. For example, previous analyses have estimated a mean vertebrate decline of more than 50% since 1970 (Living Planet Index2). Here we show, however, that this estimate is driven by less than 3% of vertebrate populations; if these extremely declining populations are excluded, the global trend switches to an increase. The sensitivity of global mean trends to outliers suggests that more informative indices are needed. We propose an alternative approach, which identifies clusters of extreme decline (or increase) that differ statistically from the majority of population trends. We show that, of taxonomic-geographic systems in the Living Planet Index, 16 systems contain clusters of extreme decline (comprising around 1% of populations; these extreme declines occur disproportionately in larger animals) and 7 contain extreme increases (around 0.4% of populations). The remaining 98.6% of populations across all systems showed no mean global trend. However, when analysed separately, three systems were declining strongly with high certainty (all in the Indo-Pacific region) and seven were declining strongly but with less certainty (mostly reptile and amphibian groups). Accounting for extreme clusters fundamentally alters the interpretation of global vertebrate trends and should be used to help to prioritize conservation efforts.

Local Adaptation to Biotic Interactions: A Meta-analysis across Latitudes.

Adaptation to local conditions can increase species' geographic distributions and rates of diversification, but which components of the environment commonly drive local adaptation-particularly the importance of biotic interactions-is unclear. Biotic interactions should drive local adaptation when they impose consistent divergent selection; if this is common, we expect transplant experiments to detect more frequent and stronger local adaptation when biotic interactions are left intact. We tested this hypothesis using a meta-analysis of transplant experiments from >125 studies (mostly of plants). Overall, local adaptation was common, and biotic interactions affected fitness. Nevertheless, local adaptation was neither more common nor stronger when biotic interactions were left intact, either between experimental treatments within studies (control vs. biotic interactions experimentally manipulated) or between studies that used natural versus biotically altered transplant environments. However, the effect of ameliorating negative interactions varied with latitude, suggesting that interactions may promote local adaptation more often in tropical than in temperate ecosystems, although few tropical studies were available to test this. Our results suggest that biotic interactions often fail to drive local adaptation even though they strongly affect fitness, perhaps because temperate biotic environments are unpredictable at the spatiotemporal scales required for local adaptation.