Mediterranean songbirds show pronounced seasonal variation in thermoregulatory traits.

Addressing the patterns of variation in thermal traits is crucial to better predict the potential effects of climate change on organisms. Here, we assessed seasonal (winter vs summer) adjustments in key thermoregulatory traits in eight Mediterranean-resident songbirds. Overall, songbirds increased whole-animal (by 8%) and mass-adjusted (by 9%) basal metabolic rate and decreased (by 56%) thermal conductance below the thermoneutral zone during winter. The magnitude of these changes was within the lower values found in songbirds from northern temperate areas. Moreover, songbirds increased (by 11%) evaporative water loss within the thermoneutral zone during summer, while its rate of increase above the inflection point of evaporative water loss (i.e., the slope of evaporative water loss versus temperature) decreased by 35% during summer - a value well above that reported for other temperate and tropical songbirds. Finally, body mass increased by 5% during winter, a pattern similar to that found in many northern temperate species. Our findings support the idea that physiological adjustments might enhance the resilience of Mediterranean songbirds to environmental changes, with short-term benefits by saving energy and water under thermally stressful conditions. Nevertheless, not all species showed the same patterns, suggesting different strategies in their thermoregulatory adaptations to seasonal environments.

Heat tolerance limits of Mediterranean songbirds and their current and future vulnerabilities to temperature extremes.

Songbirds are one of the groups most vulnerable to extreme heat events. Although several recent studies have assessed their physiological responses to heat, most of them have focused solely on arid-zone species. We investigated thermoregulatory responses to heat in eight small-sized songbirds occurring in the Mediterranean Basin, where heatwaves are becoming more frequent and intense. Specifically, we determined their heat tolerance limits (HTLs) and evaporative cooling efficiency, and evaluated their current and future vulnerabilities to heat in southwestern Iberia, a Mediterranean climate warming hotspot. To do this, we exposed birds to an increasing profile of air temperatures (Ta) and measured resting metabolic rate (RMR), evaporative water loss (EWL), evaporative cooling efficiency (the ratio between evaporative heat loss and metabolic heat production) and body temperature (Tb). HTL ranged between 40 and 46°C across species, and all species showed rapid increases in RMR, EWL and Tb in response to increasing Ta. However, only the crested lark (Galerida cristata) achieved an evaporative cooling efficiency greater than 1. The studied songbirds currently experience summer Ta maxima that surpass the upper critical temperatures of their thermoneutral zone and even their HTL. Our estimates indicate that five of the eight species will experience moderate risk of lethal dehydration by the end of the century. We argue that the limited heat tolerance and evaporative cooling efficiency of small-sized Mediterranean songbirds make them particularly vulnerable to heatwaves, which will be exacerbated under future climate change scenarios.

The thermoregulatory role of relative bill and leg surface areas in a Mediterranean population of Great tit (Parus major).

There is growing evidence on the role of legs and bill as 'thermal windows' in birds coping with heat stress. However, there is a lack of empirical work examining the relationship between the relative bill and/or leg surface areas and key thermoregulatory traits such as the limits of the thermoneutral zone (TNZ) or the cooling efficiency at high temperatures. Here, we explored this relationship in a Mediterranean population of Great tit (Parus major) facing increasing thermal stress in its environment. The lower and upper critical limits of the TNZ were found to be 17.7 ± 1.6ºC and 34.5 ± 0.7°C, respectively, and the basal metabolic rate was 0.96 ± 0.12 ml O2 min-1 on average. The evaporative water loss (EWL) inflection point was established at 31.85 ± 0.27°C and was not significantly different from the value of the upper critical limit. No significant relationship was observed between the relative bill or tarsi size and TNZ critical limits, breadth, mass-independent VO2, or mass-independent EWL at any environmental temperature (from 10 to 40°C). However, Great tit males (but not females) with larger tarsi areas (a proxy of leg surface area) showed higher cooling efficiencies at 40°C. We found no support for the hypothesis that the bill surface area plays a significant role as a thermal window in Great tits, but the leg surface areas may play a role in males' physiological responses to high temperatures. On the one hand, we argue that the studied population occupies habitats with available microclimates and fresh water for drinking during summer, so active heat dissipation by EWL might be favored instead of dry heat loss through the bill surface. Conversely, male dominance behaviors could imply a greater dependence on cutaneous EWL through the upper leg surfaces as a consequence of higher exposure to harsh environmental conditions than faced by females.

Urohidrosis as an overlooked cooling mechanism in long-legged birds.

Behavioural thermoregulation could buffer the impacts of climate warming on vertebrates. Specifically, the wetting of body surfaces and the resulting evaporation of body fluids serves as a cooling mechanism in a number of vertebrates coping with heat. Storks (Ciconiidae) frequently excrete onto their legs to prevent overheating, a phenomenon known as urohidrosis. Despite the increasingly recognised role of bare and highly vascularised body parts in heat exchange, the ecological and evolutionary determinants of urohidrosis have been largely ignored. We combine urohidrosis data from a scientifically curated media repository with microclimate and ecological data to investigate the determinants of urohidrosis in all extant stork species. Our phylogenetic generalised linear mixed models show that high temperature, humidity and solar radiation, and low wind speed, promote the use of urohidrosis across species. Moreover, species that typically forage in open landscapes exhibit a more pronounced use of urohidrosis than those mainly foraging in waterbodies. Substantial interspecific variation in temperature thresholds for urohidrosis prevalence points to different species vulnerabilities to high temperatures. This integrated approach that uses online data sources and methods to model microclimates should provide insight into animal thermoregulation and improve our capacity to make accurate predictions of climate change's impact on biodiversity.

Going to sleep with a full belly: Thermal substitution by specific dynamic action in shorebirds.

Many bird species occupy habitats where environmental temperatures fall well below their thermoneutral zone (TNZ), so they must deal with high energy costs of thermoregulation to keep in heat balance. In such circumstances, specific dynamic action (SDA) - also referred to as heat increment of feeding - could be used to substitute for these high thermoregulatory costs. If birds ingest food before going to roost in cold environments, the SDA will be beneficial as an energy-conserving mechanism by thermal substitution. We investigated the magnitude and duration of SDA in a small-sized shorebird, the dunlin Calidris alpina, while feeding on living prey. We simulated in the aviary the food availability of a semidiurnal tidal cycle, and calculated the thermal substitution by SDA below their TNZ at the beginning of the "high tide" (resting period), after feeding ad libitum during the "low tide" (feeding period). Within TNZ (25 °C), dunlins consumed 12% (2.15 kJ) of the gross energy intake in excess by the SDA, with a duration of ~95 min. At 10 °C, i.e. below the lower critical limit of TNZ, SDA magnitude and duration were reduced by 29% and 31%, respectively. The amount of food ingested significantly affected the duration and magnitude of SDA, as well as the dunlin's body temperature. Thermal substitution by SDA saved 11% of the dunlin's theoretical daily energy requirement during winter. This thermal substitution could be commonly used by birds going to roost in cold climates. Interacting with other different behavioral and/or physiological strategies would help to maintain lower energetic costs and enhance survival in cold environments.

Understanding how birds rebuild fat stores during migration: insights from an experimental study.

Mechanisms underlying fat accumulation for long-distance migration are not fully understood. This is especially relevant in the context of global change, as many migrants are dealing with changes in natural habitats and associated food sources and energy stores. The continental Black-tailed godwit Limosa limosa limosa is a long-distance migratory bird that has undergone a considerable dietary shift over the past few decades. Historically, godwits fed on an animal-based diet, but currently, during the non-breeding period godwits feed almost exclusively on rice seeds. The latter diet may allow building up of their fuel stores for migration by significantly increasing de novo lipogenesis (DNL) activity. Here, we performed an experiment to investigate lipid flux and the abundance of key enzymes involved in DNL in godwits, during fasting and refueling periods at the staging site, while feeding on rice seeds or fly larvae. Despite no significant differences found in enzymatic abundance (FASN, ME1, ACC and LPL) in stored fat, experimental godwits feeding on rice seeds presented high rates of DNL when compared to fly-larvae fed birds (~35 times more) and fasted godwits (no DNL activity). The increase of fractional DNL in godwits feeding on a carbohydrate-rich diet can potentially be enhanced by the fasting period that stimulates lipogenesis. Although requiring further testing, these recent findings provide new insights into the mechanisms of avian fat accumulation during a fasting and refueling cycle and associated responses to habitat and dietary changes in a migratory species.

Day and night use of habitats by northern pintails during winter in a primary rice-growing region of Iberia.

Loss of natural wetlands is a global phenomenon that has severe consequences for waterbird populations and their associated ecosystem services. Although agroecosystems can reduce the impact of natural habitat loss, drivers of use of such artificial habitats by waterbirds remain poorly understood. Using the cosmopolitan northern pintail Anas acuta as a model species, we monitored home-range and fine-scale resource selection across the agricultural landscape. Individuals were tracked using GPS-GSM transmitters, and a suite of environmental and landscape features were measured throughout the winter seasons. Spatial patterns of habitat use were analysed using generalized linear mixed effect models by integrating field-observations with GPS telemetry. All birds used rice fields as foraging grounds at night and commuted to an adjacent reservoir to roost during daylight. Home-ranges and maximum foraging distances of nocturnally foraging birds increased with decreasing availability of flooded fields, and were positively correlated with moonlight levels. Birds selected flooded rice paddies (water depth range: 9-21 cm) with standing stubble and substrate with pebbles smaller than 0.5 cm in diameter. Density of rice seeds, rice paddy size, and other environmental and landscape features did not emerge as significant predictors. Our findings indicate that nocturnal foraging of northern pintails within rice fields is driven primarily by straw manipulation, water level and substrate pebble size. Thus, the presence of standing stubble in flooded paddies with soft bottoms should be prioritized to improve foraging areas for dabbling ducks. These management procedures in themselves would not increase economic costs or affect rice production and could be applied for dabbling-duck conservation throughout the world.

Wetland salinity induces sex-dependent carry-over effects on the individual performance of a long-distance migrant.

Salinization is having a major impact on wetlands and its biota worldwide. Specifically, many migratory animals that rely on wetlands are increasingly exposed to elevated salinity on their nonbreeding grounds. Experimental evidence suggests that physiological challenges associated with increasing salinity may disrupt self-maintenance processes in these species. Nonetheless, the potential role of salinity as a driver of ecological carry-over effects remains unstudied. Here, we investigated the extent to which the use of saline wetlands during winter - inferred from feather stable isotope values - induces residual effects that carry over and influence physiological traits relevant to fitness in black-tailed godwits Limosa limosa limosa on their northward migration. Overwintering males and females were segregated by wetland salinity in West Africa, with females mostly occupying freshwater wetlands. The use of these wetlands along a gradient of salinities was associated with differences in immune responsiveness to phytohaemagglutinin and sized-corrected body mass in godwits staging in southern Europe during northward migration - 3,000 km from the nonbreeding grounds - but in males only. These findings provide a window onto the processes by which wetland salinity can induce carry-over effects and can help predict how migratory species should respond to future climate-induced increases in salinity.

Metabolic plasticity for subcutaneous fat accumulation in a long-distance migratory bird traced by 2H2O.

The migrant black-tailed godwit (Limosa limosa) traditionally used natural wetlands in the Iberian Peninsula to prepare for migratory flights by feeding mainly in estuaries. In recent decades, this species has become increasingly dependent on rice fields, thereby relying on a plant-based diet for fuelling. Dietary fatty acids (FA) seem to be determinant to the composition of accumulated subcutaneous fat in migratory birds. It is still unclear whether metabolic plasticity allows for modification and/or synthesis of FA, contributing to a lipid profile that enables a successful migratory performance. Deuterated water was administered to captive black-tailed godwits submitted to two diets (fly larvae versus rice) and the incorporation of deuterium (2H) into subcutaneous triglycerides was analyzed by NMR. A recently developed localized biopsy method for sampling subcutaneous fat was employed with later successful release of all birds into the wild. The average chemical structure reflected mostly a mixture of saturated and monounsaturated 16- and 18-carbon FA, a profile frequently found in migrant birds. Significantly higher levels of polyunsaturated FA, as well as detectable levels of n-3 FA, were observed in fly-larvae-fed birds. Excess 2H-enrichments in FA revealed significantly higher rates of fractional de novo lipogenesis and FA desaturation capacity in rice-fed birds. This novel and non-lethal tracer method revealed the capacity of this species to alter its lipid metabolism to compensate for a poorer dietary lipid contribution. Because of its versatility, adapting this method to other scenarios and/or other migratory species is considered feasible and cost-effective.

Physiological, Morphological and Behavioural Responses of Self-Feeding Precocial Chicks Copying with Contrasting Levels of Water Salinity during Development.

Combined physiological and behavioural responses to salt loads during development have rarely been studied in air-breathing vertebrates able to inhabit hypersaline habitats, but they may be of particular importance in understanding, for example, the differences among species in patterns of habitat use or ontogenetic diet switches. Here, we compared the physiological and behavioural responses of self-feeding precocial chicks developed in contrasting levels of water salinity. The model species was the Black-winged Stilt (Himantopus himantopus) a precocial shorebird that breeds in a range of habitats from freshwater to hypersaline wetlands. Specifically, we compared resting metabolic rate (RMR), heat shock proteins (Hsp70), plasma ions, hematocrit, body mass, body size, growth rate and head-shaking behaviour of captive-reared Black-winged Stilt fledglings developed under fresh (0 ‰), saline (20 ‰), and hypersaline (60 ‰) water. Contrary to expectations, none of the physiological and morphological variables measured differed significantly among treatments. Likewise, the RMR of wild and captive-reared fledglings was similar. Surprisingly, the saltgland mass of wild fledglings from freshwater and those from hypersaline habitats was also similar. However, head-shaking, a behavioural response associated to minimize salt intake and to expel the secretions of salt glands, differed according to salinity source: head-shaking rate increased with increasing salinity. The results of this study support the key role of behavioural osmoregulation in avoiding salt stress during development.

How salinity and temperature combine to affect physiological state and performance in red knots with contrasting non-breeding environments.

Migratory shorebirds inhabit environments that may yield contrasting salinity-temperature regimes-with widely varying osmoregulatory demands, even within a given species-and the question is: by which physiological means and at which organisational level do they show adjustments with respect to these demands? Red knots Calidris canutus winter in coastal areas over a range of latitudes. The nominal subspecies winters in salty areas in the tropics, whereas the subspecies Calidris canutus islandica winters in north-temperate regions of comparatively lower salinities and temperatures. In this study, both subspecies of red knot were acclimated to different salinity (28/40‰)-temperature (5/35 °C) combinations for 2-week periods. We then measured food/salt intakes, basal metabolic rate (BMR), body mass and temperature, fat and salt gland scores, gizzard mass, heat-shock proteins, heterophils/lymphocytes (H/L) ratio and plasma Na(+) to assess the responses of each taxon to osmoregulatory challenges. High salinity (HS)-warm-acclimated birds reduced food/salt intake, BMR, body mass, fat score and gizzard mass, showing that salt/heat loads constrained energy acquisition rates. Higher salt gland scores in saltier treatments indicated that its size was adjusted to higher osmoregulatory demands. Elevated plasma Na(+) and H/L ratio in high-salinity-warm-acclimated birds indicated that salt/heat loads might have a direct effect on the water-salt balance and stress responses of red knots. Subspecies had little or no effect on most measured parameters, suggesting that most adjustments reflect phenotypic flexibility rather than subspecific adaptations. Our results demonstrate how salinity and temperature affect various phenotypic traits in a migrant shorebird, highlighting the importance of considering these factors jointly when evaluating the environmental tolerances of air-breathing marine taxa.

Unravelling trophic subsidies of agroecosystems for biodiversity conservation: food consumption and nutrient recycling by waterbirds in Mediterranean rice fields.

Waterbirds can reallocate a considerable amount of nutrients within agricultural fields and between agriculture sites and wetlands. However their effects on biogeochemical cycles have rarely been quantified. We estimated bird numbers, diet (from stable isotope analysis), food supply, and the food consumption on rice fields by overwintering waterbirds in one of the most important areas for rice production in southwestern Europe and a key area for various migrating and resident waterbird species. Herein, we modelled the nutrient (N and P) recycling in rice fields, and their transport to reservoirs. The energy consumption by waterbirds (96,605±18,311 individuals) on rice fields during winter averaged at 89.9±39.0 kJ·m(-2), with its majority (89.9%) belonging to foraging on rice seeds. Thus, the birds removed about 26% of rice seeds leftover after harvest (estimated in 932.5±504.7 seeds·m(-2) in early winter) wherein common cranes and dabbling ducks (four species) were the most important consumers. Waterbirds foraging and roosting in the rice fields recycled more than 24.1 (1.0 kg·ha(-1)) of N and an additional 5.0 tons (0.2 kg·ha(-1)) of P in the Extremadura's rice fields during winter. Additionally, we estimated that 2.3 tons of N and 550 kg of P were removed from rice fields and transported to reservoirs. The seasonal foraging of wildlife should result in a direct benefit for rice farmers by improving nutrient recycling through defecation by waterbirds with respect to artificial fertilisation. Additionally, rice fields located in the cranes' core wintering areas can provide sufficient food supply to induce habitat shift from their traditional wintering habitat in 'dehesas' to rice fields, which causes indirect socioeconomic benefit through reduced acorn consumption by cranes. Our modelling approach may thus be especially helpful for management decisions regarding rice agroecosystems in areas which are also important for the conservation of migratory waterbirds.

Time course and metabolic costs of a humoral immune response in the little ringed plover Charadrius dubius.

Despite host defense against parasites and pathogens being considered a costly life-history trait, relatively few studies have assessed the energetic cost of immune responsiveness. Knowledge of such energetic costs may help to understand the mechanisms by which trade-offs with other demanding activities occur. The time course and associated metabolic costs of mounting a primary and secondary humoral immune response was examined in little ringed plovers Charadrius dubius challenged with sheep red blood cells. As was expected, the injection with this antigen increased the production of specific antibodies significantly, with peaks 6 d postinjection in both primary and secondary responses. At the peak of secondary antibody response, the antibody production was 29% higher than that observed during the primary response, but the difference was nonsignificant. Mounting the primary response did not significantly increase the resting metabolic rate (RMR) of birds, whereas the secondary response did by 21%, suggesting that the latter was more costly in terms of RMR. In spite of the fact that the primary response did not involve an increase in RMR, birds significantly decreased their body mass. This could imply an internal energy reallocation strategy to cope with the induced immune challenge. Last, we found that RMR and antibody production peaks were not coupled, which could help to conciliate the variable results of previous studies. Collectively, the results of this study support the hypothesis that humoral immunity, especially the secondary response, entails energetic costs that may trade-off with other physiological activities.

Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird.

Trade-offs between immune function and other physiological and behavioural processes are central in ecoimmunology, but one important problem is how to distinguish a reallocation of resources away from the immune system from a reallocation or redistribution within the immune system. While variation in baseline values of individual immune parameters is well established, studies in wild animals on multiple parameters during an immune response are lacking. It also remains to be tested whether and how immune responses correlate with baseline values that vary, for example, over the course of an annual cycle. We studied immunological responses to an endotoxin challenge in skylarks (Alauda arvensis), a partial migrant bird breeding in temperate zones. We compared birds injected with the endotoxin LPS with un-injected controls, characterizing immunological responses with leukocyte profiles, titres of lytic enzymes and natural antibodies, and concentrations of haptoglobin and heat shock proteins. We did this in five annual-cycle stages to test whether the response varied throughout the year. The endotoxin challenge affected six of 10 measured parameters. Lysis titres and proportions of heterophils increased; haptoglobin concentrations and proportions of lymphocytes, basophils and eosinophils decreased. The variable effects on different immune components demonstrate the complexity of an immune response. We found no evidence that the response differed between annual-cycle stages. The response was independent of baseline measures taken directly upon capture in the field, indicating that birds were facing no immunological ceiling when mounting an immune response. Values of five parameters collected under field conditions were significantly related to values taken under standardized laboratory conditions. We conclude that multiple parts of the immune system are modulated during an immunological response and that responses are not re-organized throughout the annual cycle.

Effects of salinity on the immune response of an 'osmotic generalist' bird.

Salt stress can suppress the immune function of fish and other aquatic animals, but such an effect has not yet been examined in air-breathing vertebrates that frequently cope with waters (and prey) of contrasting salinities. We investigated the effects of seawater salinity on the strength and cost of mounting an immune response in the dunlin Calidris alpina, a long-distance migratory shorebird that shifts seasonally from freshwater environments during the breeding season to marine environments during migration and the winter period. Phytohaemagglutinin (PHA)-induced skin swelling, basal metabolic rate (BMR), body mass, fat stores, and plasma ions were measured in dunlins acclimated to either freshwater or seawater (salinity: 0.3 and 35.0 ‰, respectively). Seawater-acclimated dunlins mounted a PHA-induced swelling response that was up to 56 % weaker than those held under freshwater conditions, despite ad libitum access to food. Freshwater-acclimated dunlins significantly increased their relative BMR 48 h after PHA injection, whereas seawater-acclimated dunlins did not. However, this differential immune and metabolic response between freshwater- and seawater-acclimated dunlins was not associated with significant changes in body mass, fat stores or plasma ions. Our results indicate that the strength of the immune response of this small-sized migratory shorebird was negatively influenced by the salinity of marine habitats. Further, these findings suggest that the reduced immune response observed under saline conditions might not be caused by an energy or nutrient limitation, and raise questions about the role of osmoregulatory hormones in the modulation of the immune system.

Plasma metabolite levels predict bird growth rates: A field test of model predictive ability.

Bird growth rates are usually derived from nonlinear relationships between age and some morphological structure, but this procedure may be limited by several factors. To date, nothing is known about the capacity of plasma metabolite profiling to predict chick growth rates. Based on laboratory-trials, we here develop predictive logistic models of body mass, and tarsus and wing length growth rates in Gull-billed Tern Gelochelidon nilotica chicks from measurements of plasma metabolite levels at different developmental stages. The predictive model obtained during the fastest growth period (at the age of 12 days) explained 65-68% of the chicks' growth rates, with fasting triglyceride level explaining most of the variation in growth rate. At the end of pre-fledging period, ß-hydroxybutyrate level was also a good predictor of growth rates. Finally, we carried out a field test to check the predictive capacity of the models in two colonies of wild Gull-billed Tern, comparing field-measured and model-predicted growth rates between groups. Both, measured and predicted growth rates, matched statistically. Plasma metabolite levels can thus be applied in comparative studies of chick growth rates when semi-precocial birds can be captured only once.

Understanding the energetic costs of living in saline environments: effects of salinity on basal metabolic rate, body mass and daily energy consumption of a long-distance migratory shorebird.

Many migratory vertebrates typically move between habitats with varying salinities during the annual cycle. These organisms clearly exhibit a remarkable phenotypic flexibility in their 'osmoregulatory machinery', but the metabolic consequences of salinity acclimatization are still not well understood. We investigated the effects of salinity on basal metabolic rate (BMR), body mass and daily energy consumption of a long-distance migratory shorebird, the dunlin (Calidris alpina), outside the breeding season. Mass-corrected BMR and daily energy consumption increased significantly by 17 and 20% between freshwater (0.3‰ NaCl) and saltwater (33.0-35.0‰ NaCl), respectively. Body mass in both captive and wild dunlins was lower (9-16%) in saline than in freshwater environments. These changes on BMR and body mass were quickly reversed by returning the birds to freshwater, suggesting that metabolic adjustment to saltwater and metabolic readjustment to freshwater are both processes that occur in a few days. Our findings support empirically that the processes of developing and maintaining an active osmoregulatory machinery are energetically expensive, and they could help to explain diet and/or habitat selection patterns along the flyway. Finally, we discuss whether body mass loss in saltwater may be a strategy to reduce maintenance cost in osmotically stressful conditions such as overwintering in marine habitats, and raise some methodological implications for studies of BMR-related outcomes using captive birds captured in saline environments.

Sex differences in digestive traits in sexually size-dimorphic birds: Insights from an assimilation efficiency experiment on black-tailed godwit.

Digestive assimilation efficiency is considered a trait with important implications for animal ecology. However, practically all studies have ignored the importance of sex differences in food assimilation efficiency (AE). Here, we investigated sex differences in dietary and physiological parameters in the Black-tailed Godwit Limosa limosa limosa feeding on rice seeds, a species with sexual dimorphism in body size and body mass. Gross daily food intake, gross energy intake, gross energy output and metabolizable energy intake did not vary significantly between sexes, but godwit females showed lower faeces energy density and higher AE than males. Mass-specific AE was similar in males and females, and the difference in AE could be attributed to the females' greater body mass. We suggest that a differential AE could play a role in explaining sex differences in habitat or micro-habitat selection during the non-breeding season in bird species with sexual dimorphism in size. Finally, we addressed the question about assimilation efficiency accuracy in models that estimate prey acquisitions by declining shorebirds as the Black-tailed Godwit.