Albatross movement suggests sensitivity to infrasound cues at sea.

The ways in which seabirds navigate over very large spatial scales remain poorly understood. While olfactory and visual information can provide guidance over short distances, their range is often limited to 100s km, far below the navigational capacity of wide-ranging animals such as albatrosses. Infrasound is a form of low-frequency sound that propagates for 1,000s km in the atmosphere. In marine habitats, its association with storms and ocean surface waves could in effect make it a useful cue for anticipating environmental conditions that favor or hinder flight or be associated with profitable foraging patches. However, behavioral responses of wild birds to infrasound remain untested. Here, we explored whether wandering albatrosses, Diomedea exulans, respond to microbarom infrasound at sea. We used Global Positioning System tracks of 89 free-ranging albatrosses in combination with acoustic modeling to investigate whether albatrosses preferentially orientate toward areas of 'loud' microbarom infrasound on their foraging trips. We found that in addition to responding to winds encountered in situ, albatrosses moved toward source regions associated with higher sound pressure levels. These findings suggest that albatrosses may be responding to long-range infrasonic cues. As albatrosses depend on winds and waves for soaring flight, infrasonic cues may help albatrosses to identify environmental conditions that allow them to energetically optimize flight over long distances. Our results shed light on one of the great unresolved mysteries in nature, navigation in seemingly featureless ocean environments.

Mismatches between phenotype and environment shape fitness at hyperlocal scales.

In the era of human-driven climate change, understanding whether behavioural buffering of temperature change is linked with organismal fitness is essential. According to the 'cost-benefit' model of thermoregulation, animals that live in environments with high frequencies of favourable thermal microclimates should incur lower thermoregulatory costs, thermoregulate more efficiently and shunt the associated savings in time and energy towards other vital tasks such as feeding, territory defence and mate acquisition, increasing fitness. Here, we explore how thermal landscapes at the scale of individual territories, physiological performance and behaviour interact and shape fitness in the southern rock agama lizard (Agama atra). We integrated laboratory assays of whole organism performance with behavioural observations in the field, fine-scale estimates of environmental temperature, and paternity assignment of offspring to test whether fitness is predicted by territory thermal quality (i.e. the number of hours that operative temperatures in a territory fall within an individual's performance breadth). Male lizards that occupied territories of low thermal quality spent more time behaviourally compensating for sub-optimal temperatures and displayed less. Further, display rate was positively associated with lizard fitness, suggesting that there is an opportunity cost to engaging in thermoregulatory behaviour that will change as climate change progresses.

Warmer and more acidic conditions enhance performance of an endemic low-shore gastropod.

Changing ocean temperatures are predicted to challenge marine organisms, especially when combined with other factors, such as ocean acidification. Acclimation, as a form of phenotypic plasticity, can moderate the consequences of changing environments for biota. Our understanding of how altered temperature and acidification together influence species' acclimation responses is, however, limited compared with that of responses to single stressors. This study investigated how temperature and acidification affect the thermal tolerance and righting speed of the girdled dogwhelk, Trochia cingulata. Whelks were acclimated for 2 weeks to combinations of three temperatures (11°C: cold, 13°C: moderate and 15°C: warm) and two pH regimes (8.0: moderate and 7.5: acidic). We measured the temperature sensitivity of the righting response by generating thermal performance curves from individual data collected at seven test temperatures and determined critical thermal minima (CTmin) and maxima (CTmax). We found that T. cingulata has a broad basal thermal tolerance range (∼38°C) and after acclimation to the warm temperature regime, both the optimal temperature for maximum righting speed and CTmax increased. Contrary to predictions, acidification did not narrow this population's thermal tolerance but increased CTmax. These plastic responses are likely driven by the predictable exposure to temperature extremes measured in the field which originate from the local tidal cycle and the periodic acidification associated with ocean upwelling in the region. This acclimation ability suggests that T. cingulata has at least some capacity to buffer the thermal changes and increased acidification predicted to occur with climate change.

Untangling the structural and molecular mechanisms underlying colour and rapid colour change in a lizard, Agama atra.

With functions as diverse as communication, protection and thermoregulation, coloration is one of the most important traits in lizards. The ability to change colour as a function of varying social and environmental conditions is thus an important innovation. While colour change is present in animals ranging from squids, to fish and reptiles, not much is known about the mechanisms behind it. Traditionally, colour change was attributed to migration of pigments, in particular melanin. More recent work has shown that the changes in nanostructural configuration inside iridophores are able to produce a wide palette of colours. However, the genetic mechanisms underlying colour, and colour change in particular, remain unstudied. Here we use a combination of transcriptomic and microscopic data to show that melanin, iridophores and pteridines are the main colour-producing mechanisms in Agama atra, and provide molecular and structural data suggesting that rapid colour change is achieved via melanin dispersal in combination with iridophore organization. This work demonstrates the power of combining genotypic (gene expression) and phenotypic (microscopy) information for addressing physiological questions, providing a basis for future studies of colour change.

Navigating through the r packages for movement.

The advent of miniaturized biologging devices has provided ecologists with unprecedented opportunities to record animal movement across scales, and led to the collection of ever-increasing quantities of tracking data. In parallel, sophisticated tools have been developed to process, visualize and analyse tracking data; however, many of these tools have proliferated in isolation, making it challenging for users to select the most appropriate method for the question in hand. Indeed, within the r software alone, we listed 58 packages created to deal with tracking data or 'tracking packages'. Here, we reviewed and described each tracking package based on a workflow centred around tracking data (i.e. spatio-temporal locations (x, y, t)), broken down into three stages: pre-processing, post-processing and analysis, the latter consisting of data visualization, track description, path reconstruction, behavioural pattern identification, space use characterization, trajectory simulation and others. Supporting documentation is key to render a package accessible for users. Based on a user survey, we reviewed the quality of packages' documentation and identified 11 packages with good or excellent documentation. Links between packages were assessed through a network graph analysis. Although a large group of packages showed some degree of connectivity (either depending on functions or suggesting the use of another tracking package), one third of the packages worked in isolation, reflecting a fragmentation in the r movement-ecology programming community. Finally, we provide recommendations for users when choosing packages, and for developers to maximize the usefulness of their contribution and strengthen the links within the programming community.

Sex-specific effects of wind on the flight decisions of a sexually dimorphic soaring bird.

In a highly dynamic airspace, flying animals are predicted to adjust foraging behaviour to variable wind conditions to minimize movement costs. Sexual size dimorphism is widespread in wild animal populations, and for large soaring birds which rely on favourable winds for energy-efficient flight, differences in morphology, wing loading and associated flight capabilities may lead males and females to respond differently to wind. However, the interaction between wind and sex has not been comprehensively tested. We investigated, in a large sexually dimorphic seabird which predominantly uses dynamic soaring flight, whether flight decisions are modulated to variation in winds over extended foraging trips, and whether males and females differ. Using GPS loggers we tracked 385 incubation foraging trips of wandering albatrosses Diomedea exulans, for which males are c. 20% larger than females, from two major populations (Crozet and South Georgia). Hidden Markov models were used to characterize behavioural states-directed flight, area-restricted search (ARS) and resting-and model the probability of transitioning between states in response to wind speed and relative direction, and sex. Wind speed and relative direction were important predictors of state transitioning. Birds were much more likely to take off (i.e. switch from rest to flight) in stronger headwinds, and as wind speeds increased, to be in directed flight rather than ARS. Males from Crozet but not South Georgia experienced stronger winds than females, and males from both populations were more likely to take-off in windier conditions. Albatrosses appear to deploy an energy-saving strategy by modulating taking-off, their most energetically expensive behaviour, to favourable wind conditions. The behaviour of males, which have higher wing loading requiring faster speeds for gliding flight, was influenced to a greater degree by wind than females. As such, our results indicate that variation in flight performance drives sex differences in time-activity budgets and may lead the sexes to exploit regions with different wind regimes.

Thermal landscape change as a driver of ectotherm responses to plant invasions.

A growing body of research demonstrates the impacts of invasive alien plants on native animals, but few studies consider thermal effects as a driver of the responses of native organisms. As invasive alien plants establish and alter the composition and arrangement of plant communities, the thermal landscapes available to ectotherms also change. Our study reviews the research undertaken to date on the thermal effects of alien plant invasions on native reptiles, amphibians, insects and arachnids. The 37 studies published between 1970 and early 2019 portray an overall detrimental effect of invasive plants on thermal landscapes, ectothermic individuals' performance and species abundance, diversity and composition. With a case study of a lizard species, we illustrate the use of thermal ecology tools in plant invasion research and test the generality of alien plant effects: changes in thermoregulation behaviour in invaded landscapes varied depending on the level of invasion and lizard traits. Together, the literature review and case study show that thermal effects of alien plants on ectotherms can be substantial albeit context-dependent. Further research should cover multiple combinations of native/invasive plant growth forms, invasion stages and ectotherm traits. More attention is also needed to test causality along the chain of effects from thermal landscapes to individuals, populations and communities.

Opportunities for behavioral rescue under rapid environmental change.

Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context-dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade-off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and "behavioral rescue" from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large-scale geographic differences in the impact of behavior on climate-impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk.

Environmental temperature alters the overall digestive energetics and differentially affects dietary protein and lipid use in a lizard.

Processing food (e.g. ingestion, digestion, assimilation) requires energy referred to as specific dynamic action (SDA) and is at least partially fuelled by oxidation of the nutrients (e.g. proteins and lipids) within the recently ingested meal. In ectotherms, environmental temperature can affect the magnitude and/or duration of the SDA, but is likely to also alter the mixture of nutrients that are oxidized to cover these costs. Here, we examined metabolic rate, gut passage time, assimilation efficiency and fuel use in the lizard Agama atra digesting cricket meals at three ecologically relevant temperatures (20, 25 and 32°C). Crickets were isotopically enriched with 13C-leucine or 13C-palmitic-acid tracers to distinguish between protein and lipid oxidation, respectively. Our results show that higher temperatures increased the magnitude of the SDA peak (by 318% between 32 and 20°C) and gut passage rate (63%), and decreased the duration of the SDA response (by 20% for males and 48% for females). Peak rate of dietary protein oxidation occurred sooner than peak lipid oxidation at all temperatures (70, 60 and 31 h earlier for 20, 25 and 32°C, respectively). Assimilation efficiency of proteins, but not lipids, was positively related to temperature. Interestingly, the SDA response exhibited a notable circadian rhythm. These results show that temperature has a pronounced effect on digestive energetics in A.atra, and that this effect differs between nutrient classes. Variation in environmental temperatures may thus alter the energy budget and nutrient reserves of these animals.

The Bogert Effect and environmental heterogeneity.

A classic question in evolutionary biology is whether behavioral flexibility hastens or hinders evolutionary change. The latter idea, that behavior reduces the number of environmental states experienced by an organism and buffers that organism against selection, has been dubbed the "Bogert Effect" after Charles Bogert, the biologist who first popularized the phenomenon using data from lizards. The Bogert Effect is pervasive when traits like body temperature, which tend to be invariant across space in species that behaviorally thermoregulate, are considered. Nevertheless, behavioral thermoregulation decreases or stops when spatial variation in operative temperature is low. We compared environmental temperatures, thermoregulatory behavior, and a suite of physiological and morphological traits between two populations of the southern rock agama (Agama atra) in South Africa that experience different climatic regimes. Individuals from both populations thermoregulated efficiently, maintaining body temperatures within their preferred temperature range throughout most of their activity cycle. Nevertheless, they differed in the thermal sensitivity of resting metabolic rate at cooler body temperatures and in morphology. Our results support the common assertion that thermoregulatory behavior may prevent divergence in traits like field-active body temperature, which are measured during periods of high environmental heterogeneity. Nevertheless, we show that other traits may be free to diverge if they are under selection during times when environments are homogenous. We argue that the importance of the Bogert Effect is critically dependent on the nature of environmental heterogeneity and will therefore be relevant to some traits and irrelevant to others in many populations.

Beyond colour: consistent variation in near infrared and solar reflectivity in sunbirds (Nectariniidae).

The visible spectrum represents a fraction of the sun's radiation, a large portion of which is within the near infrared (NIR). However, wavelengths outside of the visible spectrum that are reflected by coloured tissues have rarely been considered, despite their potential significance to thermal effects. Here, we report the reflectivity from 300 to 2100 nm of differently coloured feathers. We measured reflectivity across the UV-Vis-NIR spectra of different (a) body parts, (b) colour-producing mechanisms and (c) sexes for 252 individuals of 68 sunbird (family: Nectariniidae) species. Breast plumage was the most reflective and cap plumage the least. Female plumage had greater reflectivity than males. Carotenoid-based colours had the greatest reflectivity, followed by non-iridescent and iridescent melanin-based colours. As ordered arrays of melanin-filled organelles (melanosomes) produce iridescent colours, this suggests that nanostructuring may affect reflectance across the spectrum. Our results indicate that differently coloured feathers consistently vary in their thermal, as well as obvious visual, properties.

Effects of nutrient and water restriction on thermal tolerance: A test of mechanisms and hypotheses.

Nutritional deprivation or desiccation can influence thermal tolerance by impacting the insects' ability to evaporatively cool, maintain cell membrane integrity and conduct protective or repair processes. Recovery from chilling is also linked to the re-establishment of iono- and osmo-regulatory homeostasis. Here, using Mediterranean fruit fly (Ceratitis capitata, Diptera: Tephritidae), we manipulated water and nutrient availability to test the mechanistic expectation that changes in whole organism lipid and water content can elicit variation in cold or heat tolerance (scored as chill coma recovery time and heat knockdown time). We measured body condition (body water and lipid content) as well as heat shock protein 70 gene (hsp70) and protein (HSP70) levels. A significant reduction in body water content with water restriction did not translate into differences in chill coma recovery. When nutrient restriction was coupled with water deprivation, this resulted in a significant reduction (-54%) of heat knockdown time in females but male flies were unaffected. There was no evidence for an hsp70 or HSP70 response under any of the stress treatments and therefore no correlation with heat or cold tolerance. Heat hardening decreased all hsp levels. Therefore, although body water and total body lipid content differed between the treatment groups, the contribution of these factors to thermal tolerance was inconsistent with mechanistic expectations in heat knockdown time and insignificant for chill coma recovery. These results therefore highlight that the effects of resource restriction on thermal limits in insects are mechanistically more complex than previous models of stress resistance have suggested.

The speed and metabolic cost of digesting a blood meal depends on temperature in a major disease vector.

The energetics of processing a meal is crucial for understanding energy budgets of animals in the wild. Given that digestion and its associated costs may be dependent on environmental conditions, it is necessary to obtain a better understanding of these costs under diverse conditions and identify resulting behavioural or physiological trade-offs. This study examines the speed and metabolic costs - in cumulative, absolute and relative energetic terms - of processing a bloodmeal for a major zoonotic disease vector, the tsetse fly Glossina brevipalpis, across a range of ecologically relevant temperatures (25, 30 and 35°C). Respirometry showed that flies used less energy digesting meals faster at higher temperatures but that their starvation tolerance was reduced, supporting the prediction that warmer temperatures are optimal for bloodmeal digestion while cooler temperatures should be preferred for unfed or post-absorptive flies. (13)C-Breath testing revealed that the flies oxidized dietary glucose and amino acids within the first couple of hours of feeding and overall oxidized more dietary nutrients at the cooler temperatures, supporting the premise that warmer digestion temperatures are preferred because they maximize speed and minimize costs. An independent test of these predictions using a thermal gradient confirmed that recently fed flies selected warmer temperatures and then selected cooler temperatures as they became post-absorptive, presumably to maximize starvation resistance. Collectively these results suggest there are at least two thermal optima in a given population at any time and flies switch dynamically between optima throughout feeding cycles.

Plasticity of thermal tolerance and metabolism but not water loss in an invasive reed frog.

Phenotypic plasticity may buffer the selection pressures on organisms that inhabit novel or rapidly-changing environments. We investigated plasticity of thermal tolerance, energetic and water loss traits and their interaction with behaviour in a small-bodied, arboreal anuran (Hyperolius marmoratus Rapp, Hyperoliidae) undergoing rapid range expansion into the winter rainfall region of South Africa. After short-term exposure to three temperatures (acclimation treatments) commonly encountered in their historical and novel ranges, frogs exhibited a broad thermal tolerance range (mean±s.d.: 42.1±2.9 °C) and higher plasticity in CTmax than in CTmin. Resting metabolic rate was lowest in cold-acclimated animals, while active metabolic rates were lowest in warm-acclimated frogs, likely reflecting compensation towards energy conservation. Evaporative water loss was not significantly altered by the acclimation treatments in either resting or active animals, indicating limited plasticity in this trait compared to metabolism. Our results suggest that plasticity of temperature limits and metabolism may benefit this species in variable environments such as those encountered in its expanded range. Lack of plasticity in water loss during resting and activity suggests that these frogs rely on their high cutaneous resistance and behavioural means to buffer climate variation. This study highlights the importance of synergistic interactions between physiology and behaviour in determining amphibian responses to temperature variation.

Effects of within-generation thermal history on the flight performance of Ceratitis capitata: colder is better.

The influence of thermal history on temperature-dependent flight performance was investigated in an invasive agricultural pest insect, Ceratitis capitata (Diptera: Tephritidae). Flies were exposed to one of four developmental acclimation temperatures (Tacc: 15, 20, 25, 30°C) during their pupal stage and tested at these temperatures (Ttest) as adults using a full-factorial study design. Major factors influencing flight performance included sex, body mass, Ttest and the interaction between Ttest and Tacc. Successful flight performance increased with increasing Ttest across all acclimation groups (from 10% at 15°C to 77% at 30°C). Although Tacc did not affect flight performance independently, it did have a significant interaction effect with Ttest. Multiple comparisons showed that flies which had been acclimated to 15°C and 20°C performed better than those acclimated to 25°C and 30°C when tested at cold temperatures, but warm-acclimated flies did not outperform cold-acclimated flies at warmer temperatures. This provides partial support for the 'colder is better' hypothesis. To explain these results, several flight-related traits were examined to determine whether Tacc influenced flight performance as a consequence of changes in body or wing morphology, whole-animal metabolic rate or cytochrome c oxidase enzyme activity. Although significant effects of Tacc could be detected in several of the traits examined, with an emphasis on sex-related differences, increased flight performance could not be explained solely on the basis of changes in any of these traits. Overall, these results are important for understanding dispersal physiology despite the fact that the mechanisms of acclimation-related changes in flight performance remain unresolved.

High-resolution climate data reveal an increasing risk of warming-driven activity restriction for diurnal and nocturnal lizards.

Widespread species experience a variety of climates across their distribution, which can structure their thermal tolerance, and ultimately, responses to climate change. For ectotherms, activity is highly dependent on temperature, its variability and availability of favourable microclimates. Thermal exposure and tolerance may be structured by the availability and heterogeneity of microclimates for species living along temperature and/or precipitation gradients - but patterns and mechanisms underlying such gradients are poorly understood. We measured critical thermal limits (CTmax and CTmin) for five populations of two sympatric lizard species, a nocturnal gecko (Chondrodactylus bibronii) and a diurnal skink (Trachylepis variegata) and recorded hourly thermal variation for a year in three types of microclimate relevant to the activity of lizards (crevice, full sun and partial shade) for six sites across a precipitation gradient. Using a combination of physiological and modelling approaches, we derived warming tolerance for the present and the end of the century. In the present climate, we found an overall wider thermal tolerance for the nocturnal species relative to the diurnal species, and no variation in CTmax but variable CTmin along the precipitation gradient for both species. However, warming tolerances varied significantly over the course of the day, across months and microhabitats. The diurnal skink was most restricted in its daily activity in the three driest sites with up to six daily hours of restricted activity in the open (i.e. outside refugia) during the summer months, while the impacts for the nocturnal gecko were less severe, due to its higher CTmax and night activity. With climate change, lizards will experience more months where activity is restricted and increased exposure to high temperatures even within the more sheltered microhabitats. Together our results highlight the importance of considering the relevant spatiotemporal scale and habitat for understanding the thermal exposure of diurnal and nocturnal species.

High metabolic and water-loss rates in caterpillar aggregations: evidence against the resource-conservation hypothesis.

Several hypotheses have been proposed for explaining animal aggregation, including energy or water conservation. However, these physiological hypotheses have not been well investigated. Here, we report the effects of aggregation on metabolic ( ) and evaporative water-loss rates ( ) of the gregarious caterpillar Eutricha capensis, by comparing individuals and groups of individuals (N=10-100). Contrary to findings from previous physiological studies, we did not find an advantage to aggregation: unexpectedly, and did not decrease with increasing group size. and generally remained constant or increased in larger groups relative to individuals. The amount of water lost per unit of CO2 exchanged ( : ratio) showed a marked increase in grouped caterpillars, particularly in larger groups. Other benefits of aggregation (e.g. reduced predation or increased growth rates) likely outweigh these potential costs, because individuals of E. capensis aggregate voluntarily despite no obvious energetic or hygric advantage, and other potentially confounding group effects (e.g. increased thermoregulatory advantage or whole-animal activity) are inconsequential. The results of this study provide an important exception to physiological studies reporting enhanced energy or water conservation in animal groups.

Scaling of ear morphology across 127 bird species and its implications for hearing performance.

The dimensions of auditory structures among animals of varying body size can have implications for hearing performance. Larger animals often have a hearing range focused on lower frequencies than smaller animals, which may be explained by several anatomical mechanisms in the ear and their scaling relationships. While the effect of size on ear morphology and hearing performance has been explored in some mammals, anurans and lizards, much less is known about the scaling relationships for the single-ossicle, internally-coupled ears of birds. Using micro- and nano-CT scans of the tympanic middle and inner ears of 127 ecologically and phylogenetically diverse bird species, spanning more than 400-fold in head mass (2.3 to 950 g), we undertook phylogenetically-informed scaling analyses to test whether 12 morphological traits, of functional importance to hearing, maintain their relative proportions with increasing head mass. We then extended our analysis by regressing these morphological traits with measures of hearing sensitivity and range to better understand morphological underpinnings of hearing performance. We find that most auditory structures scale together in equal proportions, whereas columella length increases disproportionately. We also find that the size of several auditory structures is associated with increased hearing sensitivity and frequency hearing limits, while head mass did not explain these measures. Although both birds and mammals demonstrate proportional scaling between auditory structures, the consequences for hearing in each group may diverge due to unique morphological predictors of auditory performance.

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.