Comparative thermal adaptation in cicadas (Hemiptera: Cicadidae) inhabiting Mediterranean ecosystems

The thermal responses of cicadas inhabiting the Mediterranean ecosystems in Europe, North America, South Africa, and Australia are investigated. A total of 37 species and two subspecies from 17 genera representing eight tribes and three subfamilies of cicadas are investigated. The analysis includes species that are restricted to the Mediterranean ecosystem as well as those which also inhabit additional environments. The data suggest that cicadas adapt to the climate type regardless of particular types of plants within the various Mediterranean communities. Similarly, cicada thermal responses are independent of body size or taxonomic affinities. There is a wider range of body temperatures for the maximum voluntary tolerance temperature than for heat torpor or minimum flight temperatures. This diversity seems to be determined by the subdivision of the habitat used and the behavior of the species. All species possess relatively elevated heat torpor temperatures adapting to the general thermal characteristics of the Mediterranean ecosystem. The data suggest that cicadas adapt to the Mediterranean climate type regardless of the diversity of particular types of plants within the various communities, of body size or of taxonomic position.     

Thermal adaptation and diversity in tropical ecosystems: evidence from cicadas (Hemiptera, Cicadidae)

The latitudinal gradient in species diversity is a central problem in ecology. Expeditions covering approximately 16°54' of longitude and 21°4' of latitude and eight Argentine phytogeographic regions provided thermal adaptation data for 64 species of cicadas. We test whether species diversity relates to the diversity of thermal environments within a habitat. There are general patterns of the thermal response values decreasing in cooler floristic provinces and decreasing maximum potential temperature within a habitat except in tropical forest ecosystems. Vertical stratification of the plant communities leads to stratification in species using specific layers of the habitat. There is a decrease in thermal tolerances in species from the understory communities in comparison to middle level or canopy fauna. The understory Herrera umbraphila Sanborn & Heath is the first diurnally active cicada identified as a thermoconforming species. The body temperature for activity in H. umbraphila is less than and significantly different from active body temperatures of all other studied species regardless of habitat affiliation. These data suggest that variability in thermal niches within the heterogeneous plant community of the tropical forest environments permits species diversification as species adapt their physiology to function more efficiently at temperatures different from their potential competitors.     

THE EVOLUTION OF ENVIRONMENTAL TOLERANCE AND RANGE SIZE: A COMPARISON OF GEOGRAPHICALLY RESTRICTED AND WIDESPREAD MIMULUS

The geographic ranges of closely related species can vary dramatically, yet we do not fully grasp the mechanisms underlying such variation. The niche breadth hypothesis posits that species that have evolved broad environmental tolerances can achieve larger geographic ranges than species with narrow environmental tolerances. In turn, plasticity and genetic variation in ecologically important traits and adaptation to environmentally variable areas can facilitate the evolution of broad environmental tolerance. We used five pairs of western North American monkeyflowers to experimentally test these ideas by quantifying performance across eight temperature regimes. In four species pairs, species with broader thermal tolerances had larger geographic ranges, supporting the niche breadth hypothesis. As predicted, species with broader thermal tolerances also had more within‐population genetic variation in thermal reaction norms and experienced greater thermal variation across their geographic ranges than species with narrow thermal tolerances. Species with narrow thermal tolerance may be particularly vulnerable to changing climatic conditions due to lack of plasticity and insufficient genetic variation to respond to novel selection pressures. Conversely, species experiencing high variation in temperature across their ranges may be buffered against extinction due to climatic changes because they have evolved tolerance to a broad range of temperatures.     

Thermal biology mediates responses of amphibians and reptiles to habitat modification

Human activities often replace native forests with warmer, modified habitats that represent novel thermal environments for biodiversity. Reducing biodiversity loss hinges upon identifying which species are most sensitive to the environmental conditions that result from habitat modification. Drawing on case studies and a meta‐analysis, we examined whether observed and modelled thermal traits, including heat tolerances, variation in body temperatures, and evaporative water loss, explained variation in sensitivity of ectotherms to habitat modification. Low heat tolerances of lizards and amphibians and high evaporative water loss of amphibians were associated with increased sensitivity to habitat modification, often explaining more variation than non‐thermal traits. Heat tolerances alone explained 24–66% (mean = 38%) of the variation in species responses, and these trends were largely consistent across geographic locations and spatial scales. As habitat modification alters local microclimates, the thermal biology of species will likely play a key role in the reassembly of terrestrial communities.     

Influence of altitude, habitat and microhabitat on thermal adaptation of cicadas from Southwest Texas (Hemiptera: Cicadidae)

The thermal responses of 12 cicada species inhabiting Big Bend National Park, Texas, USA are investigated to determine the influence of altitude, habitat and microhabitat. The park provides an opportunity to analyze the thermal responses in animals from a variety of habitats and altitudinal gradients within a limited geographic range. The data suggest that thermal responses of cicadas are adaptations to their specific habitats. No thermal responses are significantly correlated with body size. The maximum voluntary tolerance temperature (an upper behavioral thermoregulatory point) and heat torpor temperatures show significant correlations with altitude. Variability in thermal responses can also be related to the characteristics of the microhabitat selected or the behavioral pattern of a species.     

Diurnal activity, temperature responses and endothermy in three South American cicadas (Homoptera: Cicadidae: Dorisiana bonaerensis, Quesada gigas and Fidicina mannifera)

1. 1. Measurements of body temperature (T_b) in the field demonstrated that endothermic cicadas regulate T_b by behavioral mechanisms as well as by endogenous heat production.

2. 2. The T_b of endothermically active cicadas without access to exogenous heat is approximately the same as the T_b of basking cicadas.

3. 3. Dorisiana bonaerensis (Berg) and Quesada gigas (Olivier) raise T_b in the field with the heat produced in flight.

4. 4. The thermal responses of a particular species are related to its activity patterns and habitat.

5. 5. Endothermy in cicadas may serve to uncouple reproductive behavior from environmental constraints; to circumvent possible thermoregulatory problems; to permit the utilization of habitats unavailable to strictly ectothermic cicadas; to reduce predation; and to optimize broadcast coverage and sound transmission.

     

Convergence and parallelism among cicadas of Argentina and the southwestern United States (Hemiptera: Cicadoidea)

Cicadas of the genera Derotettix in Argentina and Okanagodes in the south-western United States resemble each other in colour, live on salt-tolerant plants ( Atriplex spp. etc.), nearly match the colour of their respective host plants and produce songs above the range of avian hearing. The Argentine cicadas are smaller, but have nearly identical thermal limits for activity measured by the minimum temperature for flight (20–24 °C) and a body temperature at heat torpor (48–49 °C). The species shift activity from basking sites to shade at temperatures above 37 °C, although O .  gracilis rises to a significantly higher temperature (40.7 °C) than its congener (38.2 °C) or Derotettix (37.2 °C). The thermal tolerances are the highest reported for cicada species. A third group using halophytes in Argentina ( Babras sonorivox ) has similar temperature tolerances and is cryptically coloured. The genera are convergent with respect to morphology, coloration, body size, behaviour, habitat choice and host plant selection. The similarities of thermal tolerances and their influence on behaviour can be viewed as parallelism because the underlying mechanisms are the same in all species studied.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 281–288.     

Comparative proteomics of stenotopic caddisfly Crunoecia irrorata identifies acclimation strategies to warming

Species' ecological preferences are often deduced from habitat characteristics thought to represent more or less optimal conditions for physiological functioning. Evolution has led to stenotopic and eurytopic species, the former having decreased niche breadths and lower tolerances to environmental variability. Species inhabiting freshwater springs are often described as being stenotopic specialists, adapted to the stable thermal conditions found in these habitats. Whether due to past local adaptation these species have evolved or have lost intra‐generational adaptive mechanisms to cope with increasing thermal variability has, to our knowledge, never been investigated. By studying how the proteome of a stenotopic species changes as a result of increasing temperatures, we investigate if the absence or attenuation of molecular mechanisms is indicative of local adaptation to freshwater springs. An understanding of compensatory mechanisms is especially relevant as spring specialists will experience thermal conditions beyond their physiological limits due to climate change. In this study, the stenotopic species Crunoecia irrorata (Trichoptera: Lepidostomatidae, Curtis 1834) was acclimated to 10, 15 and 20°C for 168 hr. We constructed a homology‐based database and via liquid chromatography‐tandem mass spectrometry (LC‐MS/MS)‐based shotgun proteomics identified 1,358 proteins. Differentially abundant proteins and protein norms of reaction revealed candidate proteins and molecular mechanisms facilitating compensatory responses such as trehalose metabolism, tracheal system alteration and heat‐shock protein regulation. A species‐specific understanding of compensatory physiologies challenges the characterization of species as having narrow tolerances to environmental variability if that characterization is based on occurrences and habitat characteristics alone.     

Shifting thermal regimes influence competitive feeding and aggression dynamics of brook trout (Salvelinus fontinalis) and creek chub (Semotilus atromaculatus)

The natural distributions of freshwater fish species are limited by their thermal tolerances via physiological constraints and increased interspecific competition as temperatures shift toward the thermal optima of other syntopic species. Species may mediate stress from temperature change physiologically, behaviorally, or both; but these changes may compromise competitive advantages through effects on feeding and social behavior. In the Appalachian Mountains of North America, creek chub (Semotilus atromaculatus) are found in warm‐water and cold‐water streams and overlap in range with brook trout (Salvelinus fontinalis) across lower thermal maxima, where they compete for food and space. As stream temperatures continue to increase due to climate change, brook trout are under increasing thermal stress which may negatively affect their ability to compete with creek chub. To examine the influences of temperature on competitive interactions between these species, we observed feeding behavior, aggression, and habitat use differences at three temperatures approaching brook trout thermal maxima (18°C, 20°C, and 22°C) among dyad pairs for all combinations of species in experimental flow‐through tanks. We also examined feeding and habitat use of both species under solitary conditions. We found as temperature increased, feeding and aggression of brook trout were significantly reduced in the presence of creek chub. Creek chub pairs were more likely to occupy benthic areas and refugia while brook trout pairs used surface water more. Space use patterns significantly changed by pairing treatment. Aggression and space use shifts allowed increased exploitative and interference competition from creek chub when paired with brook trout that was not present in conspecific pairs. The decreased dominance of a top predator may lead to diverse impacts on stream community dynamics with implications for the future range restriction of brook trout and demonstrate possible mechanisms to facilitate competitive advantages of warm water generalist species under thermal stress.     

Natural history predicts patterns of thermal vulnerability in amphibians from the Atlantic Rainforest of Brazil

In the Brazilian Atlantic Rainforest (AF), amphibians (625 species) face habitat degradation leading to stressful thermal conditions that constrain animal activity (e.g., foraging and reproduction). Data on thermal ecology for these species are still scarce. We tested the hypothesis that environmental occupation affects the thermal tolerance of amphibian species more than their phylogenetic relationships. We evaluated patterns of thermal tolerance of 47 amphibian species by assessing critical thermal maxima and warming tolerances, relating these variables with ecological covariates (e.g., adult macro‐ and microhabitat and site of larval development). We used mean and maximum environmental temperature, ecological covariates, and morphological measurements in the phylogenetic generalized least squares model selection to evaluate which traits better predict thermal tolerance. We did not recover phylogenetic signal under a Brownian model; our results point to a strong association between critical thermal maxima and habitat and development site. Forest species were less tolerant to warm temperatures than open area or generalist species. Species with larvae that develop in lentic environment were more tolerant than those in lotic ones. Thus, species inhabiting forest microclimates are more vulnerable to the synergistic effect of habitat loss and climate change. We use radar charts as a quick evaluation tool for thermal risk diagnoses using aspects of natural history as axes.     

Comparative thermoregulation of sympatric endothermic and ectothermic cicadas (Homoptera: Cicadidae: Tibicen winnemanna and Tibicen chloromerus)

Measurements of body temperature in the field demonstrated that endothermic cicadas regulate body temperature by behavioral mechanisms as well as by endogenous heat production. Regression analysis suggests both endothermic and ectothermic species are thermoregulating. Body temperature of endothermically active cicadas without access to exogenous heat is approximately the same as the body temperature of basking cicadas. Tibicen winnemanna (Davis) raises body temperature in the field with the heat produced in flight or through the activation of the flight musculature without the act of flight. T. chloromerus (Walker) uses solar radiation to elevate body temperature to the level necessary for activity. The thermal responses of each species are related to its activity patterns with minimum flight temperature and shade-seeking temperatures significantly lower in the endothermic T. winnemanna. Heat torpor temperature appears to be related to the environment rather than behavior pattern. Endothermy in cicadas may serve to uncouple reproductive behavior from environmental constraints; to circumvent possible thermoregulatory problems; to permit the utilization of habitats unavailable to strictly ectothermic cicadas; to reduce predation; to optimize broadcast coverage and sound transmission; and to decrease possible acoustic interference. Accepted: 25 March 2000     

Developing environmental flow recommendations for freshwater mussels using the biological traits of species guilds

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Early response of the platypus to climate warming

Combining a climatic envelope modelling technique with more than two centuries (1800–2009) of distribution records has revealed the effects of a changing climate on the egg‐laying monotreme, the platypus, Ornithorhynchus anatinus. We show that the main factor associated with platypus occurrence switched from aquatic habitat availability (estimated by rainfall) to thermal tolerances (estimated by annual maximum temperature) in the 1960s. This correlates directly with the change in the annual maximum temperature anomaly from cooler to warmer conditions in southeastern Australia. Modelling of platypus habitat under emission scenarios (A1B, A2, B1 and B2) revealed large decreases (>30%) in thermally suitable habitat by 2070. This reduction, compounded by increasing demands for water for agriculture and potable use, suggests that there is real cause for concern over the future status of this species, and highlights the need for restoration of thermal refugia within the platypus’ modelled range.     

The range implications of lizard traits in changing environments

Aim Most predictions of species ranges are based on correlating current species localities to environmental conditions. These correlative models do not explicitly include a species' biology. In contrast, some mechanistic models link traits to energetics and population dynamics to predict species distributions. These models enable one to ask whether considering a species' biology is important for predicting its range. I implement mechanistic models to investigate how a species' morphology, physiology and life history influence its range. Location North America. Methods I compare the mechanistic model predictions with those of correlative models for eight species of North American lizards in both current environments and following a uniform 3 °C temperature warming. I then examine the implications of superimposing habitat and elevation requirements on constraints associated with environmental tolerances. Results In the mechanistic model, species with a narrower thermal range for activity are both predicted and observed to have more restricted distributions. Incorporating constraints on habitat and elevation further restricts species distributions beyond areas that are thermally suitable. While correlative models generally outperform mechanistic models at predicting current distributions, the performance of mechanistic models improves when incorporating additional factors. In response to a 3 °C temperature warming, the northward range shifts predicted by the mechanistic model vary between species according to trait differences and are of a greater extent than those predicted by correlative models. Main conclusions These findings highlight the importance of species traits for understanding the dynamics of species ranges in changing environments. The analysis demonstrates that mechanistic models may provide an important complement to correlative models for predicting range dynamics, which may underpredict climate‐induced range shifts.     

The brighter side of climate change: How local oceanography amplified a lobster boom in the Gulf of Maine

Ocean warming can drive poleward shifts of commercially important species with potentially significant economic impacts. Nowhere are those impacts greater than in the Gulf of Maine where North America's most valuable marine species, the American lobster (Homarus americanus Milne Edwards), has thrived for decades. However, there are growing concerns that regional maritime economies will suffer as monitored shallow water young‐of‐year lobsters decline and landings shift to the northeast. We examine how the interplay of ocean warming, tidal mixing, and larval behavior results in a brighter side of climate change. Since the 1980s lobster stocks have increased fivefold. We suggest that this increase resulted from a complex interplay between lobster larvae settlement behavior, climate change, and local oceanographic conditions. Specifically, postlarval sounding behavior is confined to a thermal envelope above 12°C and below 20°C. Summer thermally stratified surface waters in southwestern regions have historically been well within the settlement thermal envelope. Although surface layers are warming fastest in this region, the steep depth‐wise temperature gradient caused thermally suitable areas for larval settlement to expand only modestly. This contrasts with the northeast where strong tidal mixing prevents thermal stratification and recent ocean warming has made an expansive area of seabed more favorable for larval settlement. Recent declines in lobster settlement densities observed at shallow monitoring sites correlate with the expanded area of thermally suitable habitat associated with warmer summers. This leads us to hypothesize that the expanded area of suitable habitat may help explain strong lobster population increases in this region over the last decade and offset potential future declines. It also suggests that the fate of fisheries in a changing climate requires understanding local interaction between life stage‐specific biological thresholds and finer scale oceanographic processes.     

Desiccation tolerance in fully developed embryos of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata

In two Japanese cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata , with different habitat distributions, fully developed embryos hatch in response to high humidity due to rainfall. Despite the advantage of hatching on rainy days, this trait burdens embryos with an extra period of desiccation until the unpredictable advent of rain. We compared the ability of the fully developed embryos of these cicadas to endure periods of low humidity. Eggs were exposed to a combination of different humidities (43% and 75% relative humidity, RH) and durations (0–15 days), and then transferred to an environment with 100% RH to stimulate hatching. In both species, total hatching rates decreased as duration increased, although there was no significant effect of humidity. In C. facialis , a considerable proportion of the eggs hatched during the desiccation period, and the hatching rate was higher at 75% RH than at 43% RH. After transfer to 100% RH, most hatching occurred within a day regardless of the desiccation level. In G. nigrofuscata , no nymphs hatched during the desiccation periods. However, more eggs required more than a day after transfer to 100% RH to hatch after desiccation at 43% RH than at 75% RH. Consequently, the overall proportion of timely hatching of eggs (eggs hatching within a day of moisture supply) was higher after desiccation at 43% RH in C. facialis , but it was higher after desiccation at 75% RH in G. nigrofuscata . These different physiological responses of the two species may reflect adaptation to habitat dryness.     

Periodical cicadas use light for oviposition site selection

Organisms use incomplete information from local experience to assess the suitability of potential habitat sites over a wide range of spatial and temporal scales. Although ecologists have long recognized the importance of spatial scales in habitat selection, few studies have investigated the temporal scales of habitat selection. In particular, cues in the immediate environment may commonly provide indirect information about future habitat quality. In periodical cicadas (Magicicada spp.), oviposition site selection represents a very long-term habitat choice. Adult female cicadas insert eggs into tree branches during a few weeks in the summer of emergence, but their oviposition choices determine the underground habitats of root-feeding nymphs over the following 13 or 17 years. Here, field experiments are used to show that female cicadas use the local light environment of host trees during the summer of emergence to select long-term host trees. Light environments may also influence oviposition microsite selection within hosts, suggesting a potential behavioural mechanism for associating solar cues with host trees. In contrast, experimental nutrient enrichment of host trees did not influence cicada oviposition densities. These findings suggest that the light environments around host trees may provide a robust predictor of host tree quality in the near future. This habitat selection may influence the spatial distribution of several cicada-mediated ecological processes in eastern North American forests.     

Geographic body size variation in the periodical cicadas Magicicada: implications for life cycle divergence and local adaptation

Seven species in three species groups (Decim, Cassini and Decula) of periodical cicadas (Magicicada) occupy a wide latitudinal range in the eastern United States. To clarify how adult body size, a key trait affecting fitness, varies geographically with climate conditions and life cycle, we analysed the relationships of population mean head width to geographic variables (latitude, longitude, altitude), habitat annual mean temperature (AMT), life cycle and species differences. Within species, body size was larger in females than males and decreased with increasing latitude (and decreasing habitat AMT), following the converse Bergmann's rule. For the pair of recently diverged 13‐ and 17‐year species in each group, 13‐year cicadas were equal in size or slightly smaller on average than their 17‐year counterparts despite their shorter developmental time. This fact suggests that, under the same climatic conditions, 17‐year cicadas have lowered growth rates compared to their 13‐years counterparts, allowing 13‐year cicadas with faster growth rates to achieve body sizes equivalent to those of their 17‐year counterparts at the same locations. However, in the Decim group, which includes two 13‐year species, the more southerly, anciently diverged 13‐year species (Magicicada tredecim) was characterized by a larger body size than the other, more northerly 13‐ and 17‐year species, suggesting that local adaptation in warmer habitats may ultimately lead to evolution of larger body sizes. Our results demonstrate how geographic clines in body size may be maintained in sister species possessing different life cycles.     

Annual temperature variation influences the vulnerability of montane bird communities to land‐use change

Understanding how and why species respond to land‐use change is one of the central challenges in conservation biology, yet the causes of variation in the responses of species to land‐use change remain unclear. We tested whether adaptation to different abiotic environments influenced the vulnerability of bird communities to agricultural expansion in the Himalayan mountain range, which exhibits a strong east–west gradient in annual temperature variation. We did so by surveying bird communities in forest and agriculture at opposite ends of that gradient. We contrasted metrics of species richness, diversity, community composition and forest dependency across land‐use types and regions, and tested whether species’ thermal sensitivity influenced their response to the replacement of forest with agriculture. Agricultural land in the relatively aseasonal east harboured significantly fewer bird species than did forests, a pattern that is starkly reversed in the highly seasonal west. For species common to both regions, eastern populations used forest ~35% more than did western populations. While western species were less constrained by temperature than eastern species, western species with narrow thermal tolerances were also more forest dependent. Selection across a stark environmental gradient on a common species pool appears to have altered the vulnerability of Himalayan birds to forest loss, with communities in the relatively aseasonal east much more sensitive to forest conversion than those in the west. Adaptation to local environmental conditions appears to mediate species’ responses to land use change, with thermal specialists more vulnerable to forest loss than species with greater thermal tolerances. Species’ responses to global change may differ predictably along abiotic gradients even within a single region or biodiversity hotspot, and such variation must be addressed in conservation planning.     

Ecophysiological responses to climate change in cicadas

Cicadas are large hemipteran insects characterized by unique life‐history traits, such as extraordinarily long life cycles, a subterranean/terrestrial habitat transition, xylem sap‐feeding and melodious sound production. These fascinating features of cicadas have attracted much attention in the research fields of physiology and ecology, resulting in an accumulation of knowledge about the underlying mechanisms and their adaptive significance. Although community‐level responses to recent climate change have already been documented for cicada fauna, an understanding of their causal relationships is still at the initial stages. In this review, we summarize current knowledge about environmental adaptations of cicadas to facilitate a deeper understanding of the ecophysiological consequences of climate change. We first outline the diverse responses of cicadas to environmental factors, mainly temperature, and their strategies to cope with naturally fluctuating environments. Then, we discuss the consequence of upcoming climate change by consolidating the current findings. This review highlights the fact that fitness‐relevant activities are fine‐tuned to a species‐specific temperature optimum to achieve habitat segregation among coexisting species, implying that cicada diversity is highly susceptible to climate warming. As a result of their conspicuous large bodies and species‐specific calling songs, cicadas are promising candidates for use as bioindicator species to monitor ecological impacts of climate change. We encourage future works that continuously quantify population‐ and community‐level responses to upcoming climate change, as well as unveil mechanistic links between physiological traits and ecological consequences.