Species richness is greatest in the tropics, and much of this diversity is concentrated in mountains. Janzen proposed that reduced seasonal temperature variation selects for narrower thermal ...tolerances and limited dispersal along tropical elevation gradients Janzen DH (1967) Am Nat 101:233–249. These locally adapted traits should, in turn, promote reproductive isolation and higher speciation rates in tropical mountains compared with temperate ones. Here, we show that tropical and temperate montane stream insects have diverged in thermal tolerance and dispersal capacity, two key traits that are drivers of isolation in montane populations. Tropical species in each of three insect clades have markedly narrower thermal tolerances and lower dispersal than temperate species, resulting in significantly greater population divergence, higher cryptic diversity, higher tropical speciation rates, and greater accumulation of species over time. Our study also indicates that tropical montane species, with narrower thermal tolerance and reduced dispersal ability, will be especially vulnerable to rapid climate change.
Characterizing thermal acclimation is a common goal of eco‐physiological studies and has important implications for models of climate change and environmental adaptation. However, quantifying thermal ...acclimation in biological rate processes is not straightforward because many rates increase with temperature due to the acute effect of thermodynamics on molecular interactions. Disentangling such passive plastic responses from active acclimation responses is critical for describing patterns of thermal acclimation.
Here, we reviewed published studies and distinguished between different study designs measuring the acute (i.e. passive) and acclimated (i.e. active) effects of temperature on metabolic rate. We then developed a method to quantify and classify acclimation responses by comparing acute and acclimated Q10 values. Finally, we applied this method using meta‐analysis to characterize thermal acclimation in metabolic rates of ectothermic animals.
We reviewed 258 studies measuring thermal effects on metabolic rates, and found that a majority of these studies (74%) did not allow for quantifying the independent effects of acclimation. Such studies were more common when testing aquatic taxa and continue to be published even in recent years.
A meta‐analysis of 96 studies where acclimation could be quantified (using 1,072 Q10 values) revealed that ‘partial compensation’ was the most common acclimation response (i.e. acclimation tended to offset the passive change in metabolic rate due to acute temperature changes). However, ‘no acclimation’ and ‘inverse compensation’, in which acclimation further augmented the acute change in metabolic rate, were also common.
Acclimation responses differed among taxa, habitats and with experimental design. Amphibians and other terrestrial taxa tended to show weak acclimation responses, whereas fishes and other aquatic taxa tended to show stronger compensatory responses. Increasing how long the animal was allowed to adjust to a new test temperature increased the acclimation response, but body size did not. Acclimation responses were also stronger with longer acclimation durations.
Collectively, these results highlight the importance of using the appropriate experimental design to investigate and estimate thermal acclimation of biological rates. To facilitate and guide future studies of thermal acclimation, we end with some suggestions for designing and interpreting experiments.
A free Plain Language Summary can be found within the Supporting Information of this article.
A free Plain Language Summary can be found within the Supporting Information of this article.
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.
In high‐elevation streams, climate change is raising water temperatures, increasing the potential for oxygen limitation, and altering UV and flow regimes. How insects respond will depend on how tolerant they are of novel conditions and whether they can mitigate challenges via plasticity and adaptation. To predict specific outcomes, more research is urgently needed, and our review proposes key priorities for future work.
•Rapid climate change in mountain ecosystems will alter high-elevation insect communities.•New ecological interactions can arise from shifts in space (migration) and time (phenology).•Terrestrial and ...aquatic insect communities will be differentially affected by these changes.•New ecological interactions will drive evolutionary change in high-elevation insect communities.
Climate change is proceeding rapidly in high mountain regions worldwide. Rising temperatures will impact insect physiology and associated fitness and will shift populations in space and time, thereby altering community interactions and composition. Shifts in space are expected as insects move upslope to escape warming temperatures and shifts in time will occur with changes in phenology of resident high-elevation insects. Clearly, spatiotemporal shifts will not affect all species equally. Terrestrial insects may have more opportunities than aquatic insects to exploit microhabitats, potentially buffering them from warming. Such responses of insects to warming may also fuel evolutionary change, including hitchhiking of maladaptive alleles and genetic rescue. Together, these considerations suggest a striking restructuring of high-elevation insect communities that remains largely unstudied.
Climate warming is considered to be among the most serious of anthropogenic stresses to the environment, because it not only has direct effects on biodiversity, but it also exacerbates the harmful ...effects of other human‐mediated threats. The associated consequences are potentially severe, particularly in terms of threats to species preservation, as well as in the preservation of an array of ecosystem services provided by biodiversity. Among the most affected groups of animals are insects—central components of many ecosystems—for which climate change has pervasive effects from individuals to communities. In this contribution to the scientists' warning series, we summarize the effect of the gradual global surface temperature increase on insects, in terms of physiology, behavior, phenology, distribution, and species interactions, as well as the effect of increased frequency and duration of extreme events such as hot and cold spells, fires, droughts, and floods on these parameters. We warn that, if no action is taken to better understand and reduce the action of climate change on insects, we will drastically reduce our ability to build a sustainable future based on healthy, functional ecosystems. We discuss perspectives on relevant ways to conserve insects in the face of climate change, and we offer several key recommendations on management approaches that can be adopted, on policies that should be pursued, and on the involvement of the general public in the protection effort.
Mitochondria provide the vast majority of cellular energy available to eukaryotes. Therefore, adjustments in mitochondrial function through genetic changes in mitochondrial or nuclear-encoded genes ...might underlie environmental adaptation. Environmentally induced plasticity in mitochondrial function is also common, especially in response to thermal acclimation in aquatic systems. Here, we examined mitochondrial function in mayfly larvae (
and
spp.) from high and low elevation mountain streams during thermal acclimation to ecologically relevant temperatures. A multi-substrate titration protocol was used to evaluate different respiratory states in isolated mitochondria, along with cytochrome oxidase and citrate synthase activities. In general, maximal mitochondrial respiratory capacity and oxidative phosphorylation coupling efficiency decreased during acclimation to higher temperatures, suggesting montane insects may be especially vulnerable to rapid climate change. Consistent with predictions of the climate variability hypothesis, mitochondria from
collected at a low elevation site with highly variable daily and seasonal temperatures exhibited greater thermal tolerance than
from a high elevation site with comparatively stable temperatures. However, mitochondrial phenotypes were more resilient than whole-organism phenotypes in the face of thermal stress. These results highlight the complex relationships between mitochondrial and organismal genotypes, phenotypes and environmental adaptation. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'.
Rapid glacier recession is altering the physical conditions of headwater streams. Stream temperatures are predicted to rise and become increasingly variable, putting entire meltwater‐associated ...biological communities at risk of extinction. Thus, there is a pressing need to understand how thermal stress affects mountain stream insects, particularly where glaciers are likely to vanish on contemporary timescales. In this study, we measured the critical thermal maximum (CTMAX) of stonefly nymphs representing multiple species and a range of thermal regimes in the high Rocky Mountains, USA. We then collected RNA‐sequencing data to assess how organismal thermal stress translated to the cellular level. Our focal species included the meltwater stonefly, Lednia tumana, which was recently listed under the U.S. Endangered Species Act due to climate‐induced habitat loss. For all study species, critical thermal maxima (CTMAX > 20°C) far exceeded the stream temperatures mountain stoneflies experience (<10°C). Moreover, while evidence for a cellular stress response was present, we also observed constitutive expression of genes encoding proteins known to underlie thermal stress (i.e., heat shock proteins) even at low temperatures that reflected natural conditions. We show that high‐elevation aquatic insects may not be physiologically threatened by short‐term exposure to warm temperatures and that longer‐term physiological responses or biotic factors (e.g., competition) may better explain their extreme distributions.
Rapid glacier recession is altering the physical conditions of headwater streams. In this study, we tested the critical thermal maximum of stonefly nymphs from mountain streams in the high Rocky Mountains, USA, and linked our physiological results to gene expression under thermal stress. Critical thermal maxima exceeded the stream temperatures our focal stoneflies naturally experience and, while evidence for a cellular stress response was present, we also observed constitutive expression of genes underlying thermal stress even at cold temperatures that reflected natural conditions.
It has long been recognized that populations and species occupying different environments vary in their thermal tolerance traits. However, far less attention has been given to the impact of different ...environments on the capacity for plastic adjustments in thermal sensitivity, i.e., acclimation ability. One hypothesis is that environments characterized by greater thermal variability and seasonality should favor the evolution of increased acclimation ability compared with environments that are aseasonal or thermally stable. Additionally, organisms under selection for high heat tolerance may experience a trade-off and lose acclimation ability. Few studies have tested these non-mutually exclusive hypotheses at both broad latitudinal and local elevation scales in phylogenetically paired taxa. Here, we measure short-term acclimation ability of the critical thermal maximum (CTMAX) in closely related temperate and tropical mayflies (Ephemeroptera) and stoneflies (Plecoptera) from mountain streams at different elevations. We found that stream temperature was a good predictor of acclimation ability in mayflies, but not in stoneflies. Specifically, tropical mayflies showed reduced acclimation ability compared with their temperate counterparts. High elevation tropical mayflies had greater acclimation ability than low elevation mayflies, which reflected the wider temperature variation experienced in high elevation streams. In contrast, temperate and tropical stoneflies exhibited similar acclimation responses. We found no evidence for a trade-off between heat tolerance and acclimation ability in either taxonomic order. The acclimation response in stoneflies may reflect their temperate origin or foraging mode. In combination with previous studies showing tropical taxa have narrower thermal breadths, these results demonstrate that many lower elevation tropical aquatic insects are more vulnerable to climate warming than their temperate relatives.
Janzen's extension of the climate variability hypothesis (CVH) posits that increased seasonal variation at high latitudes should result in greater temperature overlap across elevations, and favour ...wider thermal breadths in temperate organisms compared to their tropical counterparts.
We tested these predictions by measuring stream temperatures and thermal breadths (i.e. the difference between the critical thermal maximum and minimum) of 62 aquatic insect species from temperate (Colorado, USA) and tropical (Papallacta, Ecuador) streams spanning an elevation gradient of c. 2000 m.
Temperate streams exhibited greater seasonal temperature variation and overlap across elevations than tropical streams, and as predicted, temperate aquatic insects exhibited broader thermal breadths than tropical insects. However, elevation had contrasting effects on patterns of thermal breadth. In temperate species, thermal breadth decreased with increasing elevation because CTMAX declined with elevation while CTMIN was similar across elevations. In tropical insects, by contrast, CTMAX declined less sharply than CTMIN with elevation, causing thermal breadth to increase with elevation.
These macrophysiological patterns are consistent with the narrower elevation ranges found in other tropical organisms, and they extend Janzen's CVH to freshwater streams. Furthermore, because lowland tropical aquatic insects have the narrowest thermal breadths of any region, they may be particularly vulnerable to short‐term extreme changes in stream temperature.
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Synopsis
It has long been known that the outcome of species interactions depends on the environmental context in which they occur. Climate change research has sparked a renewed interest in ...context-dependent species interactions because rapidly changing abiotic environments will cause species interactions to occur in novel contexts and researchers must incorporate this in their predictions of species’ responses to climate change. Here, we argue that predicting how the environment will alter the outcome of species interactions requires an integrative biology approach that focuses on the traits, mechanisms, and processes that bridge disciplines such as physiology, biomechanics, ecology, and evolutionary biology. Specifically, we advocate for quantifying how species differ in their tolerance and performance to both environmental challenges independent of species interactions, and in interactions with other species as a function of the environment. Such an approach increases our understanding of the mechanisms underlying outcomes of species interactions across different environmental contexts. This understanding will help determine how the outcome of species interactions affects the relative abundance and distribution of the interacting species in nature. A general theme that emerges from this perspective is that species are unable to maintain high levels of performance across different environmental contexts because of trade-offs between physiological tolerance to environmental challenges and performance in species interactions. Thus, an integrative biology paradigm that focuses on the trade-offs across environments, the physiological mechanisms involved, and how the ecological context impacts the outcome of species interactions provides a stronger framework to understand why species interactions are context dependent.
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