Will I survive? Assessing the thermal tolerance of an estuary-dependent mugilid, Chelon dumerili, in a changing climate

Sub-critical limits are viable alternatives to critical thermal limits.

There are seven species of skates (family Rajidae) found along the East Coast of the USA. All seven species are currently managed by the New England Fisheries Management Council as a single management complex extending from the Gulf of Maine to Cape Hatteras. The objective of the management plan is to ensure the long-term sustainability of fishing for each species via a trip limit approach. Two species are harvested in two distinct commercial fisheries. Northeast Fisheries Science Center trawl survey data and published literature were examined to investigate differences between the individual species in the skate complex. Each species exhibited a unique thermal and geographic range in addition to vital life history traits (e.g., age at maturity, longevity, and maximum size). Thorny Skate Amblyraja radiata and Smooth Skate Malacoraja senta have narrow thermal ranges and maintain a more northern distribution. Barndoor Skate Dipturus laevis have a moderate thermal habitat. Little Skate Leucoraja erinacea and Winter Skate L. ocellata have broad thermal ranges and are distributed throughout the management area. Limited inferences can be made about the thermal preferences of Clearnose Skate Raja eglanteria without data from south of Cape Hatteras, but they appear to have a broad thermal range within the management area. Rosette Skate L. garmani have a narrow thermal range and tend to be found in the deep offshore mid-Atlantic region. The validity of managing multiple distinct species in a complex is questioned. This example shows that a mixed-stock management strategy may be inadequate to meet the sustainability needs of each species and the associated fisheries. A management strategy focused on individual species may lead to a more efficient harvest of targeted species while allowing for the rebuilding of overfished species. Received November 8, 2011; accepted December 27, 2012

Thermal tolerance underpins most biogeographical patterns in ectothermic animals. Macroevolutionary patterns of thermal limits have been historically evaluated, but a role for the phylogenetic component in physiological variation has been neglected. Three marine zoogeographical provinces are recognized throughout the Neotropical region based on mean seawater temperature (Tm): the Brazilian (Tm = 26 °C), Argentinian (Tm = 15 °C), and Magellanic (Tm = 9 °C) provinces. Microhabitat temperature (MHT) was measured, and the upper (UL50) and lower (LL50) critical thermal limits were established for 12 eubrachyuran crab species from intertidal zones within these three provinces. A molecular phylogenetic analysis was performed by maximum likelihood using the 16S mitochondrial gene, also considering other representative species to enable comparative evaluations. We tested for: (1) phylogenetic pattern of MHT, UL50, and LL50; (2) effect of zoogeographical province on the evolution of both limits; and (3) evolutionary correlation between MHT and thermal limits. MHT and UL50 showed strong phylogenetic signal at the species level while LL50 was unrelated to phylogeny, suggesting a more plastic evolution. Province seems to have affected the evolution of thermal tolerance, and only UL50 was dependent on MHT. UL50 was similar between the two northern provinces compared to the southernmost while LL50 differed markedly among provinces. Apparently, critical limits are subject to different environmental pressures and thus manifest unique evolutionary histories. An asymmetrical macroevolutionary scenario for eubrachyuran thermal tolerance seems likely, as the critical thermal limits are differentially inherited and environmentally driven.

AimThermal physiology is commonly used in mechanistic models to predict species distribution and project distribution change. Such thermal constraints for ants are often measured under laboratory conditions as critical thermal limits (CTmax and CTmin), but have also been observed in the field as foraging thermal limits (FTmin and FTmax). Here we compared distribution projections based on ant physiological and behavioural thermal limits with their realized distributions to assess the validity of using ecophysiological models to predict species ranges over large scales.LocationGlobal.TaxonAnts.MethodsFrom published literature, we compiled a database of 148 lab‐measured critical thermal limits and 137 field‐observed foraging thermal limits for 20 ant genera distributed around the world. We projected their potential ranges using active hour thresholds by matching their thermal limits or preferred thermal breadth (incorporating thermal optima) with hourly surface temperature data. We then compared the projections against a comprehensive global database of ant distributions to assess the validity of physiologically and behaviourally based models.ResultsWe found that surface temperature plays a clear role in generic‐level ant biogeography. Projections based on foraging thermal limits were more conservative in constraining ranges to observed distributions, while projections based on critical thermal limits often overestimated ranges. Furthermore, thermal limit models can be improved by incorporating behaviourally derived thermal optima.Main conclusionsOur results suggest that temperature‐dependent activity niches and thermal optima better reveal species realized thermal niches than critical thermal limits, and hence can improve predictions of species distributions and future distribution changes under climate change.

AimThe climate variability hypothesis (CVH) states that a positive relationship may exist between the breadth of thermal tolerance range and the level of climatic variability experienced by taxa with increasing latitude, especially in terrestrial ectotherms. UnderCVH, we expected to find a correspondence between both thermal tolerance limits (CTmax andCTmin), ambient extreme temperature and the range sizes of species. We examined the validity of these predictions in a lowland tropical and a temperate tadpole assemblage.LocationLowland Neotropics (Bahia, Brazil) and Palaearctic (Iberian Peninsula and North Africa).MethodWe employed phylogenetic eigenvector regression (PVR) and Pagel's lambda to analyse phylogenetic signals inCTmax andCTmin. We used phylogenetic regression analyses (PGLS) to test the relationships between thermal limits, range size and temperature predictors (measured at the macroscale and microhabitat levels) and phy‐ANOVAto compare both the physiological traits and thermal regimen in both tropical and temperate assemblages.ResultsWe documented moderate‐to‐strong phylogenetic signal in both heat and cold tolerance. Temperate‐zone tadpoles had broader thermal tolerances than tropical ones. Thermal tolerance range was correlated with range sizes and was explained by seasonal thermal range predictors at the global scale. Both macro‐ and microclimate temperature variables provided the best predictive multivariate models of thermal limits at the global scale. Microclimatic predictors, however, were the main determinants ofCTmax andCTmin variation at the local level of tropical and temperate communities respectively.Main conclusionsThermal tolerance range increases with latitude in tadpoles due to the higher increase in cold tolerance in temperate tadpoles. At the global scale, both macro‐ and microenvironment thermal information were reliable predictors of critical thermal limits and thermal tolerance range, asCVHpredicts. However, thermal limits were best predicted by temperatures of the micro‐habitat at the regional level, thus suggesting that physiological thermal boundaries may be governed by thermal selection.

Spiny dogfish (Squalus acanthias) and smoothhound (Mustelus canis) sharks in the northwest Atlantic undergo seasonal migrations driven by changes in water temperature. However, the recognized thermal habitats of these regional populations are poorly described. Here, we report the thermal range, catch frequency with bottom temperature, and catch frequency with time of year for both shark species in Narragansett Bay, Rhode Island. Additionally, we describe levels of two thermal stress response indicators, heat-shock protein 70 and trimethylamine N-oxide, with an experimental increase in water temperature from 15 °C to 21 °C. Our results show that S. acanthias can be found in this region year-round and co-occurs with M. canis from June to November. Further, adult S. acanthias routinely inhabits colder waters than M. canis (highest catch frequencies at bottom temperatures of 10 °C and 21 °C, respectively), but both exhibit similar upper thermal ranges in this region (bottom temperatures of 22-23 °C). Additionally, acute exposure to a 6 °C increase in water temperature for 72 hours leads to a nearly threefold increase in heat-shock protein 70 levels in S. acanthias but not M. canis. Therefore, these species display differences in their thermal tolerance and stress response with experimental exposure to 21 °C, a common summer temperature in Narragansett Bay. Further, in temperature-stressed S. acanthias there is no accumulation of trimethylamine N-oxide. At the whole-organism level, elasmobranchs' trimethylamine N-oxide regulatory capacity may be limited by other factors. Alternatively, elasmobranchs may not rely on trimethylamine N-oxide as a primary thermal protective mechanism under the conditions tested. Findings from this study are in contrast with previous research conducted with elasmobranch cells in vitro that showed accumulation of trimethylamine N-oxide after thermal stress and subsequent suppression of the heat-shock protein 70 response.

ABSTRACTThe thermal ecology of ectotherm animals has gained considerable attention in the face of human-induced climate change. Particularly in aquatic species, the experimental assessment of critical thermal limits (CTmin and CTmax) may help to predict possible effects of global warming on habitat suitability and ultimately species survival. Here we present data on the thermal limits of two endemic and endangered extremophile fish species, inhabiting a geothermally heated and sulfur-rich spring system in southern Mexico: The sulfur molly (Poecilia sulphuraria) and the widemouth gambusia (Gambusia eurystoma). Besides physiological challenges induced by toxic hydrogen sulfide and related severe hypoxia during the day, water temperatures have been previously reported to exceed those of nearby clearwater streams. We now present temperature data for various locations and years in the sulfur spring complex and conducted laboratory thermal tolerance tests (CTmin and CTmax) both under normoxic and severe hypoxic conditions in both species. Average CTmax limits did not differ between species when dissolved oxygen was present. However, critical temperature (CTmax=43.2°C) in P. sulphuraria did not change when tested under hypoxic conditions, while G. eurystoma on average had a lower CTmax when oxygen was absent. Based on this data we calculated both species' thermal safety margins and used a TDT (thermal death time) model framework to relate our experimental data to observed temperatures in the natural habitat. Our findings suggest that both species live near their thermal limits during the annual dry season and are locally already exposed to temperatures above their critical thermal limits. We discuss these findings in the light of possible physiological adaptions of the sulfur-adapted fish species and the anthropogenic threats for this unique system.

Thermal tolerance in adult Mediterranean and Natal fruit flies ( Ceratitis capitata and Ceratitis rosa): Effects of age, gender and feeding status

Temperature is a primary driver to define the ecophysiological activity and performance of ectotherms. Thus, thermal tolerance limits have a profound effect in determining geographic ranges. In regions with extreme cold temperatures, lower thermal limits of species are a key physiological trait for survival. Moreover, thermal niche breadth also plays an important role in allowing organisms to withstand climatic variability and confers species with broader potential to establish in new regions. Here we study the evolution of thermal tolerance limits among Collembola (Arthropoda) and explore how they are affected by the colonization of polar environments. In addition, we test the hypothesis that globally invasive species are more eurythermal than non‐invasive ones. Critical thermal limits (CTmin and CTmax), classic measurements of thermal tolerance, were compiled from the literature and complemented with experimental assays for springtail species. Genetic data of the mitochondrial gene cytochrome oxidase subunit 1 (COI) was used to assemble a phylogeny. Our results show that polar springtails have lower CTmin and lower CTmax compared to species from temperate and tropical regions, consistent with the Polar pressure hypothesis. We found no phylogenetic signal for CTmax, but low values of phylogenetic signal for CTmin. Globally invasive species do not have significantly broader thermal tolerance breadth (CTrange) than non‐invasive ones, thus not supporting the predictions of the Eurythermality hypothesis. We conclude that polar springtails have evolved their thermal niches in order to adapt to extremely cold environments, which has led to decreasing both upper and lower thermal tolerance limits.

Phenotypic plasticity may allow ectotherms with complex life histories such as amphibians to cope with climate-driven changes in their environment. Plasticity in thermal tolerance (i.e., shifts of thermal limits via acclimation to higher temperatures) has been proposed as a mechanism to cope with warming and extreme thermal events. However, thermal tolerance and, hence, acclimation capacity, is known to vary with life stage. Using the common frog (Rana temporaria) as a model species, we measured the capacity to adjust lower (CTmin ) and upper (CTmax ) critical thermal limits at different acclimation temperatures. We calculated the acclimation response ratio as a metric to assess the stage-specific acclimation capacity at each of seven consecutive ontogenetic stages and tested whether acclimation capacity was influenced by body mass and/or age. We further examined how acclimation temperature, body mass, age, and ontogenetic stage influenced CTmin and CTmax . In the temperate population of R. temporaria that we studied, thermal tolerance and acclimation capacity were affected by the ontogenetic stage. However, acclimation capacity at both thermal limits was well below 100% at all life stages tested. The lowest and highest acclimation capacity in thermal limits was observed in young and late larvae, respectively. The relatively low acclimation capacity of young larvae highlights a clear risk of amphibian populations to ongoing climate change. Ignoring stage-specific differences in thermal physiology may drastically underestimate the climate vulnerability of species, which will hamper successful conservation actions.

Increasing drought frequency and duration pose a significant threat to fish species in dryland river systems. As ectotherms, fish thermal and hypoxia tolerances directly determine the capacity of species to persist in these environments during low flow periods when water temperatures are high and waterbodies become highly stratified. Chronic thermal stress can compound the impacts of acute hypoxic events on fish resulting in significant fish mortality; however, it is not known if all size classes are equally susceptible, or if the allometric scaling of physiological processes means some size classes are disproportionately affected. We investigated the physiological responses of Murray cod (Maccullochella peelii) over a four-fold body size range (0.2-3000g) to acute changes in water temperature and oxygen concentration following 4 weeks of acclimation to representative spring (20°C) and summer (28°C) water temperatures. We recorded maximum thermal tolerance (CT max), oxygen limited thermal tolerance (PCTmax ), lowest tolerable oxygen level (as the oxygen level at which lose equilibrium; O2,LOE), gill ventilation rates and aerial surface respiration threshold, blood oxygen transport capacity and lactate accumulation. Acclimation to elevated water temperatures improved thermal and hypoxia tolerance metrics across all size classes. However, body size significantly affected thermal and hypoxia responses. Small M. peelii were significantly less hypoxia tolerant than larger individuals, while larger fish were significantly less thermal tolerant than smaller fish. Hypoxia constrained thermal tolerance in M. peelii, with both small and large fish disproportionally compromised relative to mid-sized fish. Our findings indicate that both very small/young (larvae, fry, fingerlings) and very large/older M. peelii in dryland rivers are at significant risk from the combined impacts of a warming and drying climate and water extraction. These data will inform policy decisions that serve to balance competing demands on precious freshwater resources.

Critical thermal limits (CTmax and CTmin) decrease with elevation, with greater change in CTmin, and the risk to suffer heat and cold stress increasing at the gradient ends. A central prediction is that populations will adapt to the prevailing climatic conditions. Yet, reliable support for such expectation is scant because of the complexity of integrating phenotypic, molecular divergence and organism exposure. We examined intraspecific variation of CTmax and CTmin, neutral variation for 11 microsatellite loci, and micro‐ and macro‐temperatures in larvae from 11 populations of the Galician common frog (Rana parvipalmata) across an elevational gradient, to assess (1) the existence of local adaptation through a PST‐FST comparison, (2) the acclimation scope in both thermal limits, and (3) the vulnerability to suffer acute heat and cold thermal stress, measured at both macro‐ and microclimatic scales. Our study revealed significant microgeographic variation in CTmax and CTmin, and unexpected elevation gradients in pond temperatures. However, variation in CTmax and CTmin could not be attributed to selection because critical thermal limits were not correlated to elevation or temperatures. Differences in breeding phenology among populations resulted in exposure to higher and more variable temperatures at mid and high elevations. Accordingly, mid‐ and high‐elevation populations had higher CTmax and CTmin plasticities than lowland populations, but not more extreme CTmax and CTmin. Thus, our results support the prediction that plasticity and phenological shifts may hinder local adaptation, promoting thermal niche conservatism. This may simply be a consequence of a coupled variation of reproductive timing with elevation (the “elevation‐time axis” for temperature variation). Mid and high mountain populations of R. parvipalmata are more vulnerable to heat and cool impacts than lowland populations during the aquatic phase. All of this contradicts some of the existing predictions on adaptive thermal clines and vulnerability to climate change in elevational gradients.

Researchers and practitioners are increasingly using comparative assessments of critical thermal and physiological limits to assess the relative vulnerability of ectothermic species to extreme thermal and aridity conditions occurring under climate change. In most assessments of vulnerability, critical limits are compared across taxa exposed to different environmental and developmental conditions. However, many aspects of vulnerability should ideally be compared when species are exposed to the same environmental conditions, allowing a partitioning of sources of variation such as used in quantitative genetics. This is particularly important when assessing the importance of different types of plasticity to critical limits, using phylogenetic analyses to test for evolutionary constraints, isolating genetic variants that contribute to limits, characterizing evolutionary interactions among traits limiting adaptive responses, and when assessing the role of cross generation effects. However, vulnerability assessments based on critical thermal/physiological limits also need to take place within a context that is relevant to field conditions, which is not easily provided under controlled environmental conditions where behavior, microhabitat, stress exposure rates and other factors will differ from field conditions. There are ways of reconciling these requirements, such as by taking organisms from controlled environments and then testing their performance under field conditions (or vice versa). While comparisons under controlled environments are challenging for many taxa, assessments of critical thermal limits and vulnerability will always be incomplete unless environmental effects within and across generations are considered, and where the ecological relevance of assays measuring critical limits can be established.

Heat Tolerance of a Death Valley Pupfish (Genus Cyprinodon)

Altitudinal variation in bumble bee (Bombus) critical thermal limits