Inconsistent shifts in warming and temperature variability are linked to reduced avian fitness.

As the climate has warmed, many birds have advanced their breeding timing. However, as climate change also changes temperature distributions, breeding earlier might increase nestling exposure to either extreme heat or cold. Here, we combine >300,000 breeding records from 24 North American birds with historical temperature data to understand how exposure to extreme temperatures has changed. Average spring temperature increased since 1950 but change in timing of extremes was inconsistent in direction and magnitude; thus, populations could not track both average and extreme temperatures. Relative fitness was reduced following heatwaves and cold snaps in 11 and 16 of 24 species, respectively. Latitudinal variation in sensitivity in three widespread species suggests that vulnerability to extremes at range limits may contribute to range shifts. Our results add to evidence demonstrating that understanding individual sensitivity and its links to population level processes is critical for predicting vulnerability to changing climates.

Conserving forest insect biodiversity requires the protection of key habitat features.

Loss of insect biodiversity is widespread, and in forests habitat loss is one of the major drivers responsible. Integrative forest management must consider the preservation and promotion of key habitat features that provide essential microhabitats and resources to conserve biodiversity alongside ecosystem functions and services.

Contrasting Torpor Use by Reproductive Male Common Noctule Bats in the Laboratory and in the Field.

Metabolic processes of animals are often studied in controlled laboratory settings. However, these laboratory settings often do not reflect the animals' natural environment. Thus, results of metabolic measurements from laboratory studies must be cautiously applied to free-ranging animals. Recent technological advances in animal tracking allow detailed eco-physiological studies that reveal when, where, and how physiological measurements from the field differ from those from the laboratory. We investigated the torpor behavior of male common noctule bats (Nyctalus noctula) across different life history stages using two approaches: in controlled laboratory experiments and in the field using calibrated heart rate telemetry. We predicted that non-reproductive males would extensively use torpor to conserve energy, whereas reproductive males would reduce torpor use to promote spermatogenesis. We did not expect differences in torpor use between captive and wild animals as we simulated natural temperature conditions in the laboratory. We found that during the non-reproductive phase, both captive and free-ranging bats used torpor extensively. During reproduction, bats in captivity unexpectedly also used torpor throughout the day, while only free-ranging bats showed the expected reduction in torpor use. Thus, depending on life history stage, torpor behavior in the laboratory was markedly different from the wild. By implementing both approaches and at different life history stages, we were able to better explore the limitations of eco-physiological laboratory studies and make recommendations for when they are an appropriate proxy for natural behavior.

Linking human impacts to community processes in terrestrial and freshwater ecosystems.

Human impacts such as habitat loss, climate change and biological invasions are radically altering biodiversity, with greater effects projected into the future. Evidence suggests human impacts may differ substantially between terrestrial and freshwater ecosystems, but the reasons for these differences are poorly understood. We propose an integrative approach to explain these differences by linking impacts to four fundamental processes that structure communities: dispersal, speciation, species-level selection and ecological drift. Our goal is to provide process-based insights into why human impacts, and responses to impacts, may differ across ecosystem types using a mechanistic, eco-evolutionary comparative framework. To enable these insights, we review and synthesise (i) how the four processes influence diversity and dynamics in terrestrial versus freshwater communities, specifically whether the relative importance of each process differs among ecosystems, and (ii) the pathways by which human impacts can produce divergent responses across ecosystems, due to differences in the strength of processes among ecosystems we identify. Finally, we highlight research gaps and next steps, and discuss how this approach can provide new insights for conservation. By focusing on the processes that shape diversity in communities, we aim to mechanistically link human impacts to ongoing and future changes in ecosystems.

Flexible energy-saving strategies in female temperate-zone bats.

Torpor is characterized by an extreme reduction in metabolism and a common energy-saving strategy of heterothermic animals. Torpor is often associated with cold temperatures, but in the last decades, more diverse and flexible forms of torpor have been described. For example, tropical bat species maintain a low metabolism and heart rate at high ambient and body temperatures. We investigated whether bats (Nyctalus noctula) from the cooler temperate European regions also show this form of torpor with metabolic inhibition at high body temperatures, and whether this would be as pronounced in reproductive as in non-reproductive bats. We simultaneously measured metabolic rate, heart rate, and skin temperature in non-reproductive and pregnant females at a range of ambient temperatures. We found that they can decouple metabolic rate and heart rate from body temperature: they maintained an extremely low metabolism and heart rate when exposed to ambient temperatures changing from 0 to 32.5 °C, irrespective of reproductive status. When we simulated natural temperature conditions, all non-reproductive bats used torpor throughout the experiment. Pregnant bats used variable strategies from torpor, to maintaining normothermy, or a combination of both. Even a short torpor bout during the day saved up to 33% of the bats' total energy expenditure. Especially at higher temperatures, heart rate was a much better predictor of metabolic rate than skin temperature. We suggest that the capability to flexibly save energy across a range of ambient temperatures within and between reproductive states may be an important ability of these bats and possibly other temperate-zone heterotherms.

Climate change creates nutritional phenological mismatches.

Climate change is creating phenological mismatches between consumers and their resources. However, while the importance of nutritional quality in ecological interactions is widely appreciated, most studies of phenological mismatch focus on energy content alone. We argue that mismatches in terms of phenology and nutrition will increase with climate change.

Climate change shifts the timing of nutritional flux from aquatic insects.

Climate change can decouple resource supply from consumer demand, with the potential to create phenological mismatches driving negative consequences on fitness. However, the underlying ecological mechanisms of phenological mismatches between consumers and their resources have not been fully explored. Here, we use long-term records of aquatic and terrestrial insect biomass and egg-hatching times of several co-occurring insectivorous species to investigate temporal mismatches between the availability of and demand for nutrients that are essential for offspring development. We found that insects with aquatic larvae reach peak biomass earlier in the season than those with terrestrial larvae and that the relative availability of omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFAs) to consumers is almost entirely dependent on the phenology of aquatic insect emergence. This is due to the 4- to 34-fold greater n-3 LCPUFA concentration difference in insects emerging from aquatic as opposed to terrestrial habitats. From a long-sampled site (25 years) undergoing minimal land use conversion, we found that both aquatic and terrestrial insect phenologies have advanced substantially faster than those of insectivorous birds, shifting the timing of peak availability of n-3 LCPUFAs for birds during reproduction. For species that require n-3 LCPUFAs directly from diet, highly nutritious aquatic insects cannot simply be replaced by terrestrial insects, creating nutritional phenological mismatches. Our research findings reveal and highlight the increasing necessity of specifically investigating how nutritional phenology, rather than only overall resource availability, is changing for consumers in response to climate change.

A partial migrant relies upon a range-wide cue set but uses population-specific weighting for migratory timing.

BACKGROUND: Many birds species range over vast geographic regions and migrate seasonally between their breeding and overwintering sites. Deciding when to depart for migration is one of the most consequential life-history decisions an individual may make. However, it is still not fully understood which environmental cues are used to time the onset of migration and to what extent their relative importance differs across a range of migratory strategies. We focus on departure decisions of a songbird, the Eurasian blackbird Turdus merula, in which selected Russian and Polish populations are full migrants which travel relatively long-distances, whereas Finnish and German populations exhibit partial migration with shorter migration distances. METHODS: We used telemetry data from the four populations (610 individuals) to determine which environmental cues individuals from each population use to initiate their autumn migration. RESULTS: When departing, individuals in all populations selected nights with high atmospheric pressure and minimal cloud cover. Fully migratory populations departed earlier in autumn, at longer day length, at higher ambient temperatures, and during nights with higher relative atmospheric pressure and more supportive winds than partial migrants; however, they did not depart in higher synchrony. Thus, while all studied populations used the same environmental cues, they used population-specific and locally tuned thresholds to determine the day of departure. CONCLUSIONS: Our data support the idea that migratory timing is controlled by general, species-wide mechanisms, but fine-tuned thresholds in response to local conditions.

A songbird adjusts its heart rate and body temperature in response to season and fluctuating daily conditions.

In a seasonal world, organisms are continuously adjusting physiological processes relative to local environmental conditions. Owing to their limited heat and fat storage capacities, small animals, such as songbirds, must rapidly modulate their metabolism in response to weather extremes and changing seasons to ensure survival. As a consequence of previous technical limitations, most of our existing knowledge about how animals respond to changing environmental conditions comes from laboratory studies or field studies over short temporal scales. Here, we expanded beyond previous studies by outfitting 71 free-ranging Eurasian blackbirds (Turdus merula) with novel heart rate and body temperature loggers coupled with radio transmitters, and followed individuals in the wild from autumn to spring. Across seasons, blackbirds thermoconformed at night, i.e. their body temperature decreased with decreasing ambient temperature, but not so during daytime. By contrast, during all seasons blackbirds increased their heart rate when ambient temperatures became colder. However, the temperature setpoint at which heart rate was increased differed between seasons and between day and night. In our study, blackbirds showed an overall seasonal reduction in mean heart rate of 108 beats min-1 (21%) as well as a 1.2°C decrease in nighttime body temperature. Episodes of hypometabolism during cold periods likely allow the birds to save energy and, thus, help offset the increased energetic costs during the winter when also confronted with lower resource availability. Our data highlight that, similar to larger non-hibernating mammals and birds, small passerine birds such as Eurasian blackbirds not only adjust their heart rate and body temperature on daily timescales, but also exhibit pronounced seasonal changes in both that are modulated by local environmental conditions such as temperature. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Future trends in measuring physiology in free-living animals.

Thus far, ecophysiology research has predominantly been conducted within controlled laboratory-based environments, owing to a mismatch between the recording technologies available for physiological monitoring in wild animals and the suite of behaviours and environments they need to withstand, without unduly affecting subjects. While it is possible to record some physiological variables for free-living animals using animal-attached logging devices, including inertial-measurement, heart-rate and temperature loggers, the field is still in its infancy. In this opinion piece, we review the most important future research directions for advancing the field of 'physiologging' in wild animals, including the technological development that we anticipate will be required, and the fiscal and ethical challenges that must be overcome. Non-invasive, multi-sensor miniature devices are ubiquitous in the world of human health and fitness monitoring, creating invaluable opportunities for animal and human physiologging to drive synergistic advances. We argue that by capitalizing on the research efforts and advancements made in the development of human wearables, it will be possible to design the non-invasive loggers needed by ecophysiologists to collect accurate physiological data from free-ranging animals ethically and with an absolute minimum of impact. In turn, findings have the capacity to foster transformative advances in human health monitoring. Thus, we invite biomedical engineers and researchers to collaborate with the animal-tagging community to drive forward the advancements necessary to realize the full potential of both fields. This article is part of the theme issue 'Measuring physiology in free-living animals (Part II)'.

Birds advancing lay dates with warming springs face greater risk of chick mortality.

In response to a warming planet with earlier springs, migratory animals are adjusting the timing of essential life stages. Although these adjustments may be essential for keeping pace with resource phenology, they may prove insufficient, as evidenced by population declines in many species. However, even when species can match the tempo of climate change, other consequences may emerge when exposed to novel conditions earlier in the year. Here, using three long-term datasets on bird reproduction, daily insect availability, and weather, we investigated the complex mechanisms affecting reproductive success in an aerial insectivore, the tree swallow (Tachycineta bicolor). By examining breeding records over nearly half a century, we discovered that tree swallows have continuously advanced their egg laying by ∼3 d per decade. However, earlier-hatching offspring are now exposed to inclement weather events twice as often as they were in the 1970s. Our long-term daily insect biomass dataset shows no long-term trends over 25 y but precipitous drops in flying insect numbers on days with low ambient temperatures. Insect availability has a considerable impact on chick survival: Even a single inclement weather event can reduce offspring survival by >50%. Our results highlight the multifaceted threats that climate change poses on migrating species. The decoupling between cold snap occurrence and generally warming spring temperatures can affect reproductive success and threaten long-term persistence of populations. Understanding the exact mechanisms that endanger aerial insectivores is especially timely because this guild is experiencing the steepest and most widespread declines across North America and Europe.

Examination of Clock and Adcyap1 gene variation in a neotropical migratory passerine.

Complex behavioral traits, such as those making up a migratory phenotype, are regulated by multiple environmental factors and multiple genes. We investigated possible relationships between microsatellite variation at two candidate genes implicated in the control of migratory behavior, Clock and Adcyap1, and several aspects of migratory life-history and evolutionary divergence in the Painted Bunting (Passerina ciris), a species that shows wide variation in migratory and molting strategies across a disjunct distribution. We focused on Clock and Adcyap1 microsatellite variation across three Painted Bunting populations in Oklahoma, Louisiana, and North Carolina, and for the Oklahoma breeding population we used published migration tracking data on adult males to explore phenotypic variation in individual migratory behavior. We found no correlation between microsatellite allele size within either Clock and Adcyap1 relative to the initiation or duration of fall migration in adult males breeding in Oklahoma. We also show the lack of significant correlations with aspects of the migratory phenotype for the Louisiana population. Our research highlights the limitations of studying microsatellite allelic mutations that are of undetermined functional influence relative to complex behavioral phenotypes.

Asymmetric energetic costs in reciprocal-cross hybrids between carnivorous mice (Onychomys).

Aerobic respiration is a fundamental physiological trait dependent on coordinated interactions between gene products of the mitochondrial and nuclear genomes. Mitonuclear mismatch in interspecific hybrids may contribute to reproductive isolation by inducing reduced viability (or even complete inviability) due to increased metabolic costs. However, few studies have tested for effects of mitonuclear mismatch on respiration at the whole-organism level. We explored how hybridization affects metabolic rate in closely related species of grasshopper mice (genus Onychomys) to better understand the role of metabolic costs in reproductive isolation. We measured metabolic rate across a range of temperatures to calculate basal metabolic rate (BMR) and cold-induced metabolic rate (MRc) in O. leucogaster, O. torridus and O. arenicola, and in reciprocal F1 hybrids between the latter two species. Within the genus, we found a negative correlation between mass-specific BMR and body mass. Although O. arenicola was smaller than O. torridus, hybrids from both directions of the cross resembled O. arenicola in body mass. In contrast, hybrid BMR was strongly influenced by the direction of the cross: reciprocal F1 hybrids were different from each other but indistinguishable from the maternal species. In addition, MRc was not significantly different between hybrids and either parental species. These patterns indicate that metabolic costs are not increased in Onychomys F1 hybrids and, while exposure of incompatibilities in F2 hybrids cannot be ruled out, suggest that mitonuclear mismatch does not act as a primary barrier to gene flow. Maternal matching of BMR is suggestive of a strong effect of mitochondrial genotype on metabolism in hybrids. Together, our findings provide insight into the metabolic consequences of hybridization, a topic that is understudied in mammals.

Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity.

Once-abundant aerial insectivores, such as the Tree Swallow (Tachycineta bicolor), have declined steadily in the past several decades, making it imperative to understand all aspects of their ecology. Aerial insectivores forage on a mixture of aquatic and terrestrial insects that differ in fatty acid composition, specifically long-chain omega-3 polyunsaturated fatty acid (LCPUFA) content. Aquatic insects contain high levels of both LCPUFA and their precursor omega-3 PUFA, alpha-linolenic acid (ALA), whereas terrestrial insects contain much lower levels of both. We manipulated both the quantity and quality of food for Tree Swallow chicks in a full factorial design. Diets were either high-LCPUFA or low in LCPUFA but high in ALA, allowing us to separate the effects of direct LCPUFA in diet from the ability of Tree Swallows to convert their precursor, ALA, into LCPUFA. We found that fatty acid composition was more important for Tree Swallow chick performance than food quantity. On high-LCPUFA diets, chicks grew faster, were in better condition, and had greater immunocompetence and lower basal metabolic rates compared with chicks on both low LCPUFA diets. Increasing the quantity of high-LCPUFA diets resulted in improvements to all metrics of performance while increasing the quantity of low-LCPUFA diets only resulted in greater immunocompetence and lower metabolic rates. Chicks preferentially retained LCPUFA in brain and muscle when both food quantity and LCPUFA were limited. Our work suggests that fatty acid composition is an important dimension of aerial insectivore nutritional ecology and reinforces the importance of high-quality aquatic habitat for these declining birds.

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes.

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.