Energetic costs of raising brood in honey bee colonies are high, but heater bees are cheap.

Little is known about the energetic costs to insects of raising young. Honey bees collectively raise young, or brood, through a series of complex behaviors that appear to accelerate and synchronize the timing of brood maturation. These include maintaining the brood nest at warmer and consistent temperatures (33-36 °C) and the exceptional activity of heater bees. Heater bees are a part of the larger group of nurse bees that care for brood by rapidly contracting thoracic muscles to generate high body temperatures, from 42 to 47 °C. Heater bees move among brood cells and display this behavior to regulate the temperatures of individual larvae and pupae. We constructed three sets of experimental hives to explore the energy costs of raising brood in general and the cost of heater bees specifically. One set was designed to estimate the numerical allocation of individuals to the heater bee task. The second set was designed to contain only brood, which eliminated foraging and allowed us to quantify stored honey use when rearing juveniles at 10 and 30 °C. The final set was used to measure the respiration rates and energy expenditure of individual bees displaying resting, walking, heating, and agitated behavior. By integrating honey used by brood-only experimental colonies with whole-colony measurements of honey storage in the literature, we estimated that raising brood costs colonies half of their annual energy budgets stored as honey, or approximately 43.7 ± 0.9 kg·yr-1. We estimated that roughly 2 % of individuals in a colony perform as heater bees. Respiration rates of heater bees (19 mW) were more than those of resting bees (8 mW) but similar to those of walking bees (20 mW) and about half of those that were agitated (46 mW). The energetic cost of heating was more than an order of magnitude lower than the reported values for the energetic cost of flying. By integrating data from our three experimental hives, we estimate that the annual cost of raising brood is relatively high. However, heater bee behavior and physiology may require only about 7 % of the annual honey stored by a colony.

Mechanisms underlying thermal breadth differ by species in insects from adjacent but thermally distinct streams - A test of the climate variability hypothesis.

The Climate Variability Hypothesis (CVH) predicts that ectotherms from thermally variable climates should have wider thermal tolerances than their counterparts living in stable climates. Although the CVH has been widely supported, the mechanisms underlying wider tolerance traits remain unclear. We test the CVH along with three mechanistic hypotheses that may explain how differences in tolerance limits arise: 1) Short-term Acclimation Hypothesis (mechanism: rapid, reversible plasticity), 2) Long-term Effects Hypothesis (mechanisms: developmental plasticity, epigenetics, maternal effects, or adaptation), and 3) Trade-off Hypothesis (mechanism: trade-off between short- and long-term responses). We tested these hypotheses by measuring CTMIN, CTMAX, and thermal breadths (CTMAX - CTMIN) of aquatic mayfly and stonefly nymphs from adjacent streams with distinctly different levels of thermal variation following acclimation to either cool, control, and warm conditions. In one stream, daily mean temperature varied by about 5 °C annually, whereas in the other, it varied by more than 25 °C. In support of the CVH, we found that mayfly and stonefly nymphs from the thermally variable stream had broader thermal tolerances than those from the thermally stable stream. However, support for the mechanistic hypotheses differed by species. Mayflies appear to rely on long-term strategies for maintaining broader thermal limits, whereas stoneflies achieve broader thermal limits via short-term plasticity. We found no support for the Trade-off Hypothesis.

Going with the flow - how a stream insect, Pteronarcys californica, exploits local flows to increase oxygen availability.

For insects, life in water is challenging because oxygen supply is typically low compared with in air. Oxygen limitation may occur when oxygen levels or water flows are low or when warm temperatures stimulate metabolic demand for oxygen. A potential mechanism for mitigating oxygen shortages is behavior - moving to cooler, more oxygenated or faster flowing microhabitats. Whether stream insects can make meaningful choices, however, depends on: (i) how temperature, oxygen and flow vary at microspatial scales and (ii) the ability of insects to sense and exploit that variation. To assess the extent of microspatial variation in conditions, we measured temperature, oxygen saturation and flow velocity within riffles of two streams in Montana, USA. In the lab, we then examined preferences of nymphs of the stonefly Pteronarcys californica to experimental gradients based on field-measured values. Temperature and oxygen level varied only slightly within stream riffles. By contrast, flow velocity was highly heterogeneous, often varying by more than 125 cm s-1 within riffles and 44 cm s-1 around individual cobbles. Exploiting micro-variation in flow may thus be the most reliable option for altering rates of oxygen transport. In support of this prediction, P. californica showed little ability to exploit gradients in temperature and oxygen but readily exploited micro-variation in flow - consistently choosing higher flows when conditions were warm or hypoxic. These behaviors may help stream insects mitigate low-oxygen stress from climate change and other anthropogenic disturbances.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

Plasticity of salmonfly (Pteronarcys californica) respiratory phenotypes in response to changes in temperature and oxygen.

Like all taxa, populations of aquatic insects may respond to climate change by evolving new physiologies or behaviors, shifting their range, exhibiting physiological and behavioral plasticity, or going extinct. We evaluated the importance of plasticity by measuring changes in growth, survival and respiratory phenotypes of salmonfly nymphs (the stonefly Pteronarcys californica) in response to experimental combinations of dissolved oxygen and temperature. Overall, smaller individuals grew more rapidly during the 6-week experimental period, and oxygen and temperature interacted to affect growth in complex ways. Survival was lower for the warm treatment, although only four mortalities occurred (91.6% versus 100%). Nymphs acclimated to warmer temperatures did not have higher critical thermal maxima (CTmax), but those acclimated to hypoxia had CTmax values (in normoxia) that were higher by approximately 1°C. These results suggest possible adaptive plasticity of systems for taking up or delivering oxygen. We examined these possibilities by measuring the oxygen sensitivity of metabolic rates and the morphologies of tracheal gill tufts located ventrally on thoracic segments. Mass-specific metabolic rates of individuals acclimated to warmer temperatures were higher in acute hypoxia but lower in normoxia, regardless of their recent history of oxygen exposure during acclimation. The morphology of gill filaments, however, changed in ways that appeared to depress rates of oxygen delivery in functional hypoxia. Our combined results from multiple performance metrics indicate that rising temperatures and hypoxia may interact to magnify the risks to aquatic insects, but that physiological plasticity in respiratory phenotypes may offset some of these risks.

Physiology: Neutral buoyancy by an insect.

Larval phantom midges are remarkably adept at maintaining neutral buoyancy in water. A new study reveals that they do so using a previously unknown mechanism - modifying the volumes of internal air sacs using pH-driven changes in a protein embedded in the air-sac walls.

Information theory in vertebrate stress physiology.

Information theory has been applied productively across biology, but it has been used minimally in endocrinology. Here, we advocate for the integration of information theory into stress endocrinology. Presently, the majority of models of stress center on the regulation of hormone concentrations, even though what interests most endocrinologists and matters in terms of individual health and evolutionary fitness is the information content of hormones. In neuroscience, the free energy principle, a concept offered to explain how the brain infers current and future states of the environment, could be a guide for resolving how information is instantiated in hormones such as the glucocorticoids. Here, we offer several ideas and promising options for research addressing how hormones encode and cells respond to information in glucocorticoids.

Extended phenotypes: buffers or amplifiers of climate change?

Historic approaches to understanding biological responses to climate change have viewed climate as something external that happens to organisms. Organisms, however, at least partially influence their own climate experience by moving within local mosaics of microclimates. Such behaviors are increasingly being incorporated into models of species distributions and climate sensitivity. Less attention has focused on how organisms alter microclimates via extended phenotypes: phenotypes that extend beyond the organismal surface, including structures that are induced or built. We argue that predicting the consequences of climate change for organismal performance and fitness will depend on understanding the expression and consequences of extended phenotypes, the microclimatic niches they generate, and the power of plasticity and evolution to shape those niches.

Pervasive effects of Wolbachia on host activity.

Heritable symbionts have diverse effects on the physiology, reproduction and fitness of their hosts. Maternally transmitted Wolbachia are one of the most common endosymbionts in nature, infecting about half of all insect species. We test the hypothesis that Wolbachia alter host behaviour by assessing the effects of 14 different Wolbachia strains on the locomotor activity of nine Drosophila host species. We find that Wolbachia alter the activity of six different host genotypes, including all hosts in our assay infected with wRi-like Wolbachia strains (wRi, wSuz and wAur), which have rapidly spread among Drosophila species in about the last 14 000 years. While Wolbachia effects on host activity were common, the direction of these effects varied unpredictably and sometimes depended on host sex. We hypothesize that the prominent effects of wRi-like Wolbachia may be explained by patterns of Wolbachia titre and localization within host somatic tissues, particularly in the central nervous system. Our findings support the view that Wolbachia have wide-ranging effects on host behaviour. The fitness consequences of these behavioural modifications are important for understanding the evolution of host-symbiont interactions, including how Wolbachia spread within host populations.

Flow increases tolerance of heat and hypoxia of an aquatic insect.

Recent experiments support the idea that upper thermal limits of aquatic insects arise, at least in part, from a lack of sufficient oxygen: rising temperatures typically stimulate metabolic demand for oxygen more than they increase rates of oxygen supply from the environment. Consequently, factors influencing oxygen supply, like water flow, should also affect thermal and hypoxia tolerance. We tested this hypothesis by measuring the effects of experimentally manipulated flows on the heat and hypoxia tolerance of aquatic nymphs of the giant salmonfly (Plecoptera: Pteronarcys californica), a common stonefly in western North America. As predicted, stoneflies in flowing water (10 cm s-1) tolerated water that was approximately 4°C warmer and that contained approximately 15% less oxygen than did those in standing water. Our results imply that the impacts of climate change on streamflow, such as changes in patterns of precipitation and decreased snowpack, will magnify the threats to aquatic insects from warmer water temperatures and lower oxygen levels.

Metamorphosis in an Era of Increasing Climate Variability.

Most animals have complex life cycles including metamorphosis or other discrete life stage transitions, during which individuals may be particularly vulnerable to environmental stressors. With climate change, individuals will be exposed to increasing thermal and hydrologic variability during metamorphosis, which may affect survival and performance through physiological, behavioral, and ecological mechanisms. Furthermore, because metamorphosis entails changes in traits and vital rates, it is likely to play an important role in how populations respond to increasing climate variability. To identify mechanisms underlying population responses and associated trait and life history evolution, we need new approaches to estimating changes in individual traits and performance throughout metamorphosis, and we need to integrate metamorphosis as an explicit life stage in analytical models.

Temperature dependence of metabolic rate in tropical and temperate aquatic insects: Support for the Climate Variability Hypothesis in mayflies but not stoneflies.

A fundamental gap in climate change vulnerability research is an understanding of the relative thermal sensitivity of ectotherms. Aquatic insects are vital to stream ecosystem function and biodiversity but insufficiently studied with respect to their thermal physiology. With global temperatures rising at an unprecedented rate, it is imperative that we know how aquatic insects respond to increasing temperature and whether these responses vary among taxa, latitudes, and elevations. We evaluated the thermal sensitivity of standard metabolic rate in stream-dwelling baetid mayflies and perlid stoneflies across a ~2,000 m elevation gradient in the temperate Rocky Mountains in Colorado, USA, and the tropical Andes in Napo, Ecuador. We used temperature-controlled water baths and microrespirometry to estimate changes in oxygen consumption. Tropical mayflies generally exhibited greater thermal sensitivity in metabolism compared to temperate mayflies; tropical mayfly metabolic rates increased more rapidly with temperature and the insects more frequently exhibited behavioral signs of thermal stress. By contrast, temperate and tropical stoneflies did not clearly differ. Varied responses to temperature among baetid mayflies and perlid stoneflies may reflect differences in evolutionary history or ecological roles as herbivores and predators, respectively. Our results show that there is physiological variation across elevations and species and that low-elevation tropical mayflies may be especially imperiled by climate warming. Given such variation among species, broad generalizations about the vulnerability of tropical ectotherms should be made more cautiously.

Phylogenomic Resolution of Sea Spider Diversification through Integration of Multiple Data Classes.

Despite significant advances in invertebrate phylogenomics over the past decade, the higher-level phylogeny of Pycnogonida (sea spiders) remains elusive. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. Previous efforts based on a handful of genes have yielded unstable tree topologies. Here, we inferred the relationships of 89 sea spider species using targeted capture of the mitochondrial genome, 56 conserved exons, 101 ultraconserved elements, and 3 nuclear ribosomal genes. We inferred molecular divergence times by integrating morphological data for fossil species to calibrate 15 nodes in the arthropod tree of life. This integration of data classes resolved the basal topology of sea spiders with high support. The enigmatic family Austrodecidae was resolved as the sister group to the remaining Pycnogonida and the small-bodied family Rhynchothoracidae as the sister group of the robust-bodied family Pycnogonidae. Molecular divergence time estimation recovered a basal divergence of crown group sea spiders in the Ordovician. Comparison of diversification dynamics with other marine invertebrate taxa that originated in the Paleozoic suggests that sea spiders and some crustacean groups exhibit resilience to mass extinction episodes, relative to mollusk and echinoderm lineages.

Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms.

Both oxygen and temperature are fundamental factors determining metabolic performance, fitness, ecological niches, and responses of many aquatic organisms to climate change. Despite the importance of physical and physiological constraints on oxygen supply affecting aerobic metabolism of aquatic ectotherms, ecological theories such as the metabolic theory of ecology have focused on the effects of temperature rather than oxygen. This gap currently impedes mechanistic models from accurately predicting metabolic rates (i.e., oxygen consumption rates) of aquatic organisms and restricts predictions to resting metabolism, which is less affected by oxygen limitation. Here, we expand on models of metabolic scaling by accounting for the role of oxygen availability and temperature on both resting and active metabolic rates. Our model predicts that oxygen limitation is more likely to constrain metabolism in larger, warmer, and active fish. Consequently, active metabolic rates are less responsive to temperature than are resting metabolic rates, and metabolism scales to body size with a smaller exponent whenever temperatures or activity levels are higher. Results from a metaanalysis of fish metabolic rates are consistent with our model predictions. The observed interactive effects of temperature, oxygen availability, and body size predict that global warming will limit the aerobic scope of aquatic ectotherms and may place a greater metabolic burden on larger individuals, impairing their physiological performance in the future. Our model reconciles the metabolic theory with empirical observations of oxygen limitation and provides a formal, quantitative framework for predicting both resting and active metabolic rate and hence aerobic scope of aquatic ectotherms.

Key rules of life and the fading cryosphere: Impacts in alpine lakes and streams.

Alpine regions are changing rapidly due to loss of snow and ice in response to ongoing climate change. While studies have documented ecological responses in alpine lakes and streams to these changes, our ability to predict such outcomes is limited. We propose that the application of fundamental rules of life can help develop necessary predictive frameworks. We focus on four key rules of life and their interactions: the temperature dependence of biotic processes from enzymes to evolution; the wavelength dependence of the effects of solar radiation on biological and ecological processes; the ramifications of the non-arbitrary elemental stoichiometry of life; and maximization of limiting resource use efficiency across scales. As the cryosphere melts and thaws, alpine lakes and streams will experience major changes in temperature regimes, absolute and relative inputs of solar radiation in ultraviolet and photosynthetically active radiation, and relative supplies of resources (e.g., carbon, nitrogen, and phosphorus), leading to nonlinear and interactive effects on particular biota, as well as on community and ecosystem properties. We propose that applying these key rules of life to cryosphere-influenced ecosystems will reduce uncertainties about the impacts of global change and help develop an integrated global view of rapidly changing alpine environments. However, doing so will require intensive interdisciplinary collaboration and international cooperation. More broadly, the alpine cryosphere is an example of a system where improving our understanding of mechanistic underpinnings of living systems might transform our ability to predict and mitigate the impacts of ongoing global change across the daunting scope of diversity in Earth's biota and environments.

Insects in high-elevation streams: Life in extreme environments imperiled by climate change.

Climate change is altering conditions in high-elevation streams worldwide, with largely unknown effects on resident communities of aquatic insects. Here, we review the challenges of climate change for high-elevation aquatic insects and how they may respond, focusing on current gaps in knowledge. Understanding current effects and predicting future impacts will depend on progress in three areas. First, we need better descriptions of the multivariate physical challenges and interactions among challenges in high-elevation streams, which include low but rising temperatures, low oxygen supply and increasing oxygen demand, high and rising exposure to ultraviolet radiation, low ionic strength, and variable but shifting flow regimes. These factors are often studied in isolation even though they covary in nature and interact in space and time. Second, we need a better mechanistic understanding of how physical conditions in streams drive the performance of individual insects. Environment-performance links are mediated by physiology and behavior, which are poorly known in high-elevation taxa. Third, we need to define the scope and importance of potential responses across levels of biological organization. Short-term responses are defined by the tolerances of individuals, their capacities to perform adequately across a range of conditions, and behaviors used to exploit local, fine-scale variation in abiotic factors. Longer term responses to climate change, however, may include individual plasticity and evolution of populations. Whether high-elevation aquatic insects can mitigate climatic risks via these pathways is largely unknown.

There is plenty of room at the bottom: microclimates drive insect vulnerability to climate change.

Climate warming impacts biological systems profoundly. Climatologists deliver predictions about warming amplitude at coarse scales. Nevertheless, insects are small, and it remains unclear how much of the warming at coarse scales appears in the microclimates where they live. We propose a simple method for determining the pertinent spatial scale of insect microclimates. Recent studies have quantified the ability of forest understory to buffer thermal extremes, but these microclimates typically are characterized at spatial scales much larger than those determined by our method. Indeed, recent evidence supports the idea that insects can be thermally adapted even to fine scale microclimatic patterns, which can be highly variable. Finally, we discuss how microhabitat surfaces may buffer or magnify the amplitude of climate warming.

Body Size of Temperate Sea Spiders: No Evidence of Oxygen-Temperature Limitations.

AbstractOxygen limitation has been proposed as one of the key factors that limits body size at high temperatures (the oxygen-temperature hypothesis). Geographic patterns in body size are thought to be driven in part by the effects of temperature on oxygen supply and demand, particularly when the increased oxygen demand of tissues at higher temperatures outpaces the ability of large organisms to supply internal tissues with oxygen. We tested the effects of temperature on the rate of oxygen consumption of two temperate sea spider (Pycnogonida) species, Achelia chelata and Achelia gracilipes, across a range of body sizes. We measured oxygen consumption at 5 temperatures: 12, 16, 20, 24, and 28 °C. Oxygen consumption of both species increased significantly with temperature, but the effect did not depend on body size; thus, we found no evidence to support the oxygen-temperature hypothesis. While previous interspecific studies on Antarctic pycnogonids have found that larger-bodied animals have more porous cuticles, thus potentially offsetting their higher aerobic metabolic demand by increasing oxygen diffusivity, the pore area of the cuticle of the two temperate species did not change with body size. This suggests that the generally small size of warm-water sea spiders may be due to selective factors other than oxygen limitation.