Greater vulnerability to warming of marine versus terrestrial ectotherms.

Understanding which species and ecosystems will be most severely affected by warming as climate change advances is important for guiding conservation and management. Both marine and terrestrial fauna have been affected by warming1,2 but an explicit comparison of physiological sensitivity between the marine and terrestrial realms has been lacking. Assessing how close populations live to their upper thermal limits has been challenging, in part because extreme temperatures frequently drive demographic responses3,4 and yet fauna can use local thermal refugia to avoid extremes5-7. Here we show that marine ectotherms experience hourly body temperatures that are closer to their upper thermal limits than do terrestrial ectotherms across all latitudes-but that this is the case only if terrestrial species can access thermal refugia. Although not a direct prediction of population decline, this thermal safety margin provides an index of the physiological stress caused by warming. On land, the smallest thermal safety margins were found for species at mid-latitudes where the hottest hourly body temperatures occurred; by contrast, the marine species with the smallest thermal safety margins were found near the equator. We also found that local extirpations related to warming have been twice as common in the ocean as on land, which is consistent with the smaller thermal safety margins at sea. Our results suggest that different processes will exacerbate thermal vulnerability across these two realms. Higher sensitivities to warming and faster rates of colonization in the marine realm suggest that extirpations will be more frequent and species turnover faster in the ocean. By contrast, terrestrial species appear to be more vulnerable to loss of access to thermal refugia, which would make habitat fragmentation and changes in land use critical drivers of species loss on land.

Temperature dependence of competitive ability is cold-shifted compared to that of growth rate in marine phytoplankton.

The effect of climate warming on community composition is expected to be contingent on competitive outcomes, yet approaches to projecting ecological outcomes often rely on measures of density-independent performance across temperatures. Recent theory suggests that the temperature response of competitive ability differs in shape from that of population growth rate. Here, we test this hypothesis empirically and find thermal performance curves of competitive ability in aquatic microorganisms to be systematically left-shifted and flatter compared to those of exponential growth rate. The minimum resource requirement for growth, R*-an inverse indicator of competitive ability-changes with temperature following a U-shaped pattern in all four species tested, contrasting from their left-skewed density-independent growth rate thermal performance curves. Our results provide new evidence that exploitative competitive success is highest at temperatures that are sub-optimal for growth, suggesting performance estimates of density-independent variables might underpredict performance in cooler competitive environments.

Bringing traits back into the equation: A roadmap to understand species redistribution.

Ecological and evolutionary theories have proposed that species traits should be important in mediating species responses to contemporary climate change; yet, empirical evidence has so far provided mixed evidence for the role of behavioral, life history, or ecological characteristics in facilitating or hindering species range shifts. As such, the utility of trait-based approaches to predict species redistribution under climate change has been called into question. We develop the perspective, supported by evidence, that trait variation, if used carefully can have high potential utility, but that past analyses have in many cases failed to identify an explanatory value for traits by not fully embracing the complexity of species range shifts. First, we discuss the relevant theory linking species traits to range shift processes at the leading (expansion) and trailing (contraction) edges of species distributions and highlight the need to clarify the mechanistic basis of trait-based approaches. Second, we provide a brief overview of range shift-trait studies and identify new opportunities for trait integration that consider range-specific processes and intraspecific variability. Third, we explore the circumstances under which environmental and biotic context dependencies are likely to affect our ability to identify the contribution of species traits to range shift processes. Finally, we propose that revealing the role of traits in shaping species redistribution may likely require accounting for methodological variation arising from the range shift estimation process as well as addressing existing functional, geographical, and phylogenetic biases. We provide a series of considerations for more effectively integrating traits as well as extrinsic and methodological factors into species redistribution research. Together, these analytical approaches promise stronger mechanistic and predictive understanding that can help society mitigate and adapt to the effects of climate change on biodiversity.

Data rescue: saving environmental data from extinction.

Historical and long-term environmental datasets are imperative to understanding how natural systems respond to our changing world. Although immensely valuable, these data are at risk of being lost unless actively curated and archived in data repositories. The practice of data rescue, which we define as identifying, preserving, and sharing valuable data and associated metadata at risk of loss, is an important means of ensuring the long-term viability and accessibility of such datasets. Improvements in policies and best practices around data management will hopefully limit future need for data rescue; these changes, however, do not apply retroactively. While rescuing data is not new, the term lacks formal definition, is often conflated with other terms (i.e. data reuse), and lacks general recommendations. Here, we outline seven key guidelines for effective rescue of historically collected and unmanaged datasets. We discuss prioritization of datasets to rescue, forming effective data rescue teams, preparing the data and associated metadata, and archiving and sharing the rescued materials. In an era of rapid environmental change, the best policy solutions will require evidence from both contemporary and historical sources. It is, therefore, imperative that we identify and preserve valuable, at-risk environmental data before they are lost to science.

Biological sensitivities to high-resolution climate change projections in the California current marine ecosystem.

The California Current Marine Ecosystem is a highly productive system that exhibits strong natural variability and vulnerability to anthropogenic climate trends. Relating projections of ocean change to biological sensitivities requires detailed synthesis of experimental results. Here, we combine measured biological sensitivities with high-resolution climate projections of key variables (temperature, oxygen, and pCO2 ) to identify the direction, magnitude, and spatial distribution of organism-scale vulnerabilities to multiple axes of projected ocean change. Among 12 selected species of cultural and economic importance, we find that all are sensitive to projected changes in ocean conditions through responses that affect individual performance or population processes. Response indices were largest in the northern region and inner shelf. While performance traits generally increased with projected changes, fitness traits generally decreased, indicating that concurrent stresses can lead to fitness loss. For two species, combining sensitivities to temperature and oxygen changes through the Metabolic Index shows how aerobic habitat availability could be compressed under future conditions. Our results suggest substantial and specific ecological susceptibility in the next 80 years, including potential regional loss of canopy-forming kelp, changes in nearshore food webs caused by declining rates of survival among red urchins, Dungeness crab, and razor clams, and loss of aerobic habitat for anchovy and pink shrimp. We also highlight fillable gaps in knowledge, including specific physiological responses to stressors, variation in responses across life stages, and responses to multistressor combinations. These findings strengthen the case for filling information gaps with experiments focused on fitness-related responses and those that can be used to parameterize integrative physiological models, and suggest that the CCME is susceptible to substantial changes to ecosystem structure and function within this century.

Predicting the fate of eDNA in the environment and implications for studying biodiversity.

Environmental DNA (eDNA) applications are transforming the standard of characterizing aquatic biodiversity via the presence, location and abundance of DNA collected from environmental samples. As eDNA studies use DNA fragments as a proxy for the presence of organisms, the ecological properties of the complex and dynamic environments from which eDNA is sampled need to be considered for accurate biological interpretation. In this review, we discuss the role that differing environments play on the major processes that eDNA undergoes between organism and collection, including shedding, decay and transport. We focus on a mechanistic understanding of these processes and highlight how decay and transport models are being developed towards more accurate and robust predictions of the fate of eDNA. We conclude with five recommendations for eDNA researchers and practitioners, to advance current best practices, as well as to support a future model of eDNA spatio-temporal persistence.

Metabolic Theory and the Temperature-Size Rule Explain the Temperature Dependence of Population Carrying Capacity.

The temperature dependence of highly conserved subcellular metabolic systems affects ecological patterns and processes across scales, from organisms to ecosystems. Population density at carrying capacity plays an important role in evolutionary processes, biodiversity, and ecosystem function, yet how it varies with temperature-dependent metabolism remains unclear. Though the exponential effect of temperature on intrinsic population growth rate, r, is well known, we still lack clear evidence that population density at carrying capacity, K, declines with increasing per capita metabolic rate, as predicted by the metabolic theory of ecology (MTE). We experimentally tested whether temperature effects on photosynthesis propagate directly to population carrying capacity in a model species, the mobile phytoplankton Tetraselmis tetrahele. After maintaining populations at a fixed resource supply and fixed temperatures for 43 days, we found that carrying capacity declined with increasing temperature. This decline was predicted quantitatively when models included temperature-dependent metabolic rates and temperature-associated body-size shifts. Our results demonstrate that warming reduces carrying capacity and that temperature effects on body size and metabolic rate interact to determine how temperature affects population dynamics. These findings bolster efforts to relate metabolic temperature dependence to population and ecosystem patterns via MTE.

Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment.

As thermal regimes change worldwide, projections of future population and species persistence often require estimates of how population growth rates depend on temperature. These projections rarely account for how temporal variation in temperature can systematically modify growth rates relative to projections based on constant temperatures. Here, we tested the hypothesis that time-averaged population growth rates in fluctuating thermal environments differ from growth rates in constant conditions as a consequence of Jensen's inequality, and that the thermal performance curves (TPCs) describing population growth in fluctuating environments can be predicted quantitatively based on TPCs generated in constant laboratory conditions. With experimental populations of the green alga Tetraselmis tetrahele, we show that nonlinear averaging techniques accurately predicted increased as well as decreased population growth rates in fluctuating thermal regimes relative to constant thermal regimes. We extrapolate from these results to project critical temperatures for population growth and persistence of 89 phytoplankton species in naturally variable thermal environments. These results advance our ability to predict population dynamics in the context of global change.

Sperm Bindin Divergence under Sexual Selection and Concerted Evolution in Sea Stars.

Selection associated with competition among males or sexual conflict between mates can create positive selection for high rates of molecular evolution of gamete recognition genes and lead to reproductive isolation between species. We analyzed coding sequence and repetitive domain variation in the gene encoding the sperm acrosomal protein bindin in 13 diverse sea star species. We found that bindin has a conserved coding sequence domain structure in all 13 species, with several repeated motifs in a large central region that is similar among all sea stars in organization but highly divergent among genera in nucleotide and predicted amino acid sequence. More bindin codons and lineages showed positive selection for high relative rates of amino acid substitution in genera with gonochoric outcrossing adults (and greater expected strength of sexual selection) than in selfing hermaphrodites. That difference is consistent with the expectation that selfing (a highly derived mating system) may moderate the strength of sexual selection and limit the accumulation of bindin amino acid differences. The results implicate both positive selection on single codons and concerted evolution within the repetitive region in bindin divergence, and suggest that both single amino acid differences and repeat differences may affect sperm-egg binding and reproductive compatibility.

Warming-Induced Changes to Body Size Stabilize Consumer-Resource Dynamics.

Both body size and temperature directly influence consumer-resource dynamics. There is also widespread empirical evidence for the temperature-size rule (TSR), which creates a negative relationship between temperature and body size. However, it is not known how the TSR affects community dynamics. Here we integrate temperature- and size-dependent models to include indirect effects of warming, through changes in body size, to answer the question, How does the TSR affect the predicted response of consumer-resource systems to warming? We find that the TSR is expected to maintain consumer-resource biomass ratios and buffer the community from extinctions under warming. While our results are limited to conditions where organisms are below their thermal optimum, they hold under a range of realistic temperature-size responses and are robust to the type of functional response. Our analyses suggest that the widely observed TSR may reduce the impacts of warming on consumer-resource systems.

Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation.

Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.

Species traits and climate velocity explain geographic range shifts in an ocean-warming hotspot.

Species' ranges are shifting globally in response to climate warming, with substantial variability among taxa, even within regions. Relationships between range dynamics and intrinsic species traits may be particularly apparent in the ocean, where temperature more directly shapes species' distributions. Here, we test for a role of species traits and climate velocity in driving range extensions in the ocean-warming hotspot of southeast Australia. Climate velocity explained some variation in range shifts, however, including species traits more than doubled the variation explained. Swimming ability, omnivory and latitudinal range size all had positive relationships with range extension rate, supporting hypotheses that increased dispersal capacity and ecological generalism promote extensions. We find independent support for the hypothesis that species with narrow latitudinal ranges are limited by factors other than climate. Our findings suggest that small-ranging species are in double jeopardy, with limited ability to escape warming and greater intrinsic vulnerability to stochastic disturbances.

Ocean acidification through the lens of ecological theory.

Ocean acidification, chemical changes to the carbonate system of seawater, is emerging as a key environmental challenge accompanying global warming and other human-induced perturbations. Considerable research seeks to define the scope and character of potential outcomes from this phenomenon, but a crucial impediment persists. Ecological theory, despite its power and utility, has been only peripherally applied to the problem. Here we sketch in broad strokes several areas where fundamental principles of ecology have the capacity to generate insight into ocean acidification's consequences. We focus on conceptual models that, when considered in the context of acidification, yield explicit predictions regarding a spectrum of population- and community-level effects, from narrowing of species ranges and shifts in patterns of demographic connectivity, to modified consumer-resource relationships, to ascendance of weedy taxa and loss of species diversity. Although our coverage represents only a small fraction of the breadth of possible insights achievable from the application of theory, our hope is that this initial foray will spur expanded efforts to blend experiments with theoretical approaches. The result promises to be a deeper and more nuanced understanding of ocean acidification'and the ecological changes it portends.

Harnessing open science practices to teach ecology and evolutionary biology using interactive tutorials.

Open science skills are increasingly important for a career in ecology and evolutionary biology (EEB) as efforts to make data and analyses publicly available continue to become more commonplace. While learning core concepts in EEB, students are also expected to gain skills in conducting open science to prepare for future careers. Core open science skills like programming, data sharing, and practices that promote reproducibility can be taught to undergraduate students alongside core concepts in EEB. Yet, these skills are not always taught in biology undergraduate programs, and a major challenge in developing open science skills and learning EEB concepts simultaneously is the high cognitive load associated with learning multiple disparate concepts at the same time. One solution is to provide students with easily digestible, scaffolded, pre-formatted code in the form of vignettes and interactive tutorials. Here, we present six open source teaching tutorials for undergraduate students in EEB. These tutorials teach fundamental ecological concepts, data literacy, programming (using R software), and analysis skills using publicly available datasets while introducing students to open science concepts and tools. Spanning a variety of EEB topics and skill levels, these tutorials serve as examples and resources for educators to integrate open science tools, programming, and data literacy into teaching EEB at the undergraduate level.

Climate drives global functional trait variation in lizards.

A major challenge in ecology and evolution is to disentangle the mechanisms driving broad-scale variation in biological traits such as body size, colour, thermal physiology traits and behaviour. Climate has long been thought to drive trait evolution and abiotic filtering of trait variation in ectotherms because their thermal performance and fitness are closely related to environmental conditions. However, previous studies investigating climatic variables associated with trait variation have lacked a mechanistic description of the underpinning processes. Here, we use a mechanistic model to predict how climate affects thermal performance of ectotherms and thereby the direction and strength of the effect of selection on different functional traits. We show that climate drives macro-evolutionary patterns in body size, cold tolerance and preferred body temperatures among lizards, and that trait variation is more constrained in regions where selection is predicted to be stronger. These findings provide a mechanistic explanation for observations on how climate drives trait variation in ectotherms through its effect on thermal performance. By connecting physical, physiological and macro-evolutionary principles, the model and results provide an integrative, mechanistic framework for predicting organismal responses to present climates and climate change.

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.

Global analysis of thermal tolerance and latitude in ectotherms.

A tenet of macroecology is that physiological processes of organisms are linked to large-scale geographical patterns in environmental conditions. Species at higher latitudes experience greater seasonal temperature variation and are consequently predicted to withstand greater temperature extremes. We tested for relationships between breadths of thermal tolerance in ectothermic animals and the latitude of specimen location using all available data, while accounting for habitat, hemisphere, methodological differences and taxonomic affinity. We found that thermal tolerance breadths generally increase with latitude, and do so at a greater rate in the Northern Hemisphere. In terrestrial ectotherms, upper thermal limits vary little while lower thermal limits decrease with latitude. By contrast, marine species display a coherent poleward decrease in both upper and lower thermal limits. Our findings provide comprehensive global support for hypotheses generated from studies at smaller taxonomic subsets and geographical scales. Our results further indicate differences between terrestrial and marine ectotherms in how thermal physiology varies with latitude that may relate to the degree of temperature variability experienced on land and in the ocean.

The evolution of critical thermal limits of life on Earth.

Understanding how species' thermal limits have evolved across the tree of life is central to predicting species' responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary 'attractors' that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change.

Life in fluctuating environments.

Variability in the environment defines the structure and dynamics of all living systems, from organisms to ecosystems. Species have evolved traits and strategies that allow them to detect, exploit and predict the changing environment. These traits allow organisms to maintain steady internal conditions required for physiological functioning through feedback mechanisms that allow internal conditions to remain at or near a set-point despite a fluctuating environment. In addition to feedback, many organisms have evolved feedforward processes, which allow them to adjust in anticipation of an expected future state of the environment. Here we provide a framework describing how feedback and feedforward mechanisms operating within organisms can generate effects across scales of organization, and how they allow living systems to persist in fluctuating environments. Daily, seasonal and multi-year cycles provide cues that organisms use to anticipate changes in physiologically relevant environmental conditions. Using feedforward mechanisms, organisms can exploit correlations in environmental variables to prepare for anticipated future changes. Strategies to obtain, store and act on information about the conditional nature of future events are advantageous and are evidenced in widespread phenotypes such as circadian clocks, social behaviour, diapause and migrations. Humans are altering the ways in which the environment fluctuates, causing correlations between environmental variables to become decoupled, decreasing the reliability of cues. Human-induced environmental change is also altering sensory environments and the ability of organisms to detect cues. Recognizing that living systems combine feedback and feedforward processes is essential to understanding their responses to current and future regimes of environmental fluctuations. This article is part of the theme issue 'Integrative research perspectives on marine conservation'.