Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming.
TL;DR: An integrative, synthetic approach including the investigation of multiple physiological traits (metabolic performance and thermal tolerance), and their plasticity, is proposed to provide more accurate and balanced predictions on species and assemblage vulnerability to both acute and chronic effects of global warming.
Abstract: Predicting species vulnerability to global warming requires a comprehensive, mechanistic understanding of sublethal and lethal thermal tolerances. To date, however, most studies investigating species physiological responses to increasing temperature have focused on the underlying physiological traits of either acute or chronic tolerance in isolation. Here we propose an integrative, synthetic approach including the investigation of multiple physiological traits (metabolic performance and thermal tolerance), and their plasticity, to provide more accurate and balanced predictions on species and assemblage vulnerability to both acute and chronic effects of global warming. We applied this approach to more accurately elucidate relative species vulnerability to warming within an assemblage of six caridean prawns occurring in the same geographic, hence macroclimatic, region, but living in different thermal habitats. Prawns were exposed to four incubation temperatures (10, 15, 20 and 25 °C) for 7 days, their metabolic rates and upper thermal limits were measured, and plasticity was calculated according to the concept of Reaction Norms, as well as Q10 for metabolism. Compared to species occupying narrower/more stable thermal niches, species inhabiting broader/more variable thermal environments (including the invasive Palaemon macrodactylus) are likely to be less vulnerable to extreme acute thermal events as a result of their higher upper thermal limits. Nevertheless, they may be at greater risk from chronic exposure to warming due to the greater metabolic costs they incur. Indeed, a trade-off between acute and chronic tolerance was apparent in the assemblage investigated. However, the invasive species P. macrodactylus represents an exception to this pattern, showing elevated thermal limits and plasticity of these limits, as well as a high metabolic control. In general, integrating multiple proxies for species physiological acute and chronic responses to increasing temperature helps providing more accurate predictions on species vulnerability to warming.
Citations
More filters
TL;DR: This analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures, and proposes that limited potential for behavioural plasticity favours the evolution of greater plasticity in physiological traits, consistent with the ‘Bogert effect’.
Abstract: Global warming is increasing the overheating risk for many organisms, though the potential for plasticity in thermal tolerance to mitigate this risk is largely unknown. In part, this shortcoming stems from a lack of knowledge about global and taxonomic patterns of variation in tolerance plasticity. To address this critical issue, we test leading hypotheses for broad-scale variation in ectotherm tolerance plasticity using a dataset that includes vertebrate and invertebrate taxa from terrestrial, freshwater and marine habitats. Contrary to expectation, plasticity in heat tolerance was unrelated to latitude or thermal seasonality. However, plasticity in cold tolerance is associated with thermal seasonality in some habitat types. In addition, aquatic taxa have approximately twice the plasticity of terrestrial taxa. Based on the observed patterns of variation in tolerance plasticity, we propose that limited potential for behavioural plasticity (i.e. behavioural thermoregulation) favours the evolution of greater plasticity in physiological traits, consistent with the ‘Bogert effect’. Finally, we find that all ectotherms have relatively low acclimation in thermal tolerance and demonstrate that overheating risk will be minimally reduced by acclimation in even the most plastic groups. Our analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures.
538 citations
TL;DR: Empirical evidence suggests that populations and species from more variable environments show higher levels of plasticity that might preadapt them to extremes, but genetic variance for plastic responses can also be low, and genetic variation may not be expressed for some classes of traits under extreme conditions.
Abstract: Phenotypic plasticity, if adaptive, may allow species to counter the detrimental effects of extreme conditions, but the infrequent occurrence of extreme environments and/or their restriction to low-quality habitats within a species range means that they exert little direct selection on reaction norms. Plasticity could, therefore, be maladaptive under extreme environments, unless genetic correlations are strong between extreme and non-extreme environmental states, and the optimum phenotype changes smoothly with the environment. Empirical evidence suggests that populations and species from more variable environments show higher levels of plasticity that might preadapt them to extremes, but genetic variance for plastic responses can also be low, and genetic variation may not be expressed for some classes of traits under extreme conditions. Much of the empirical literature on plastic responses to extremes has not yet been linked to ecologically relevant conditions, such as asymmetrical fluctuations in the case of temperature extremes. Nevertheless, evolved plastic responses are likely to be important for natural and agricultural species increasingly exposed to climate extremes, and there is an urgent need to collect empirical information and link this to model predictions.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.
257 citations
15 Jun 2012
TL;DR: The fourth assessment report (AR4) of the Intergovernmental Panel on Climate Change (IPCC) which was completed in 2007 stated that: "Warming of the climate system is unequivocal, as is now evident from observations of increases in global average air and ocean temperatures, widespread melting of snow and ice, and rising global average sea level".
Abstract: The Fourth Assessment Report (AR4) of the Intergovernmental Panel on Climate Change (IPCC), which was completed in 2007 stated that: “Warming of the climate system is unequivocal, as is now evident from observations of increases in global average air and ocean temperatures, widespread melting of snow and ice, and rising global average sea level.” It also stated that observational evidence from all continents and most oceans shows that many natural systems are being affected by regional climate changes, particularly in increases in temperature. Significantly, the AR4 found that since the mid-twentieth century most of the observed increase in global average temperatures is very likely due to the observed increase in anthropogenic greenhouse gas concentrations. When the term “very likely” is used in this context, it denotes a probability level of 90 per cent or higher.
251 citations
TL;DR: The evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris, is quantified and Rapid evolution of carbon‐use efficiency provides a potentially general mechanism for thermal adaptation in phy toplankon and implies that evolutionary responses in phytochemical cycles will modify biogeochemical cycles and hence food web structure and function under warming.
Abstract: Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited.
249 citations
Cites background from "Integrating metabolic performance, ..."
...…(Yvon-Durocher et al. 2011), and shifts in the distribution of traits (e.g. body size, metabolic rates, stoichiometry) via phenotypic plasticity (Schaum et al. 2013; Magozzi & Calosi 2014) and rapid evolution (Lohbeck et al. 2012; Schaum & Collins 2014; Schl€uter et al. 2014; Geerts et al. 2015)....
[...]
TL;DR: This review shows that, apart from the stress response mediated by heat shock proteins, the physiological mechanisms of heat tolerance in insects remain poorly studied, and emphasizes the importance of incorporating physiological information for modelling species distributions and ecological interactions under global warming scenarios.
Abstract: Surviving changing climate conditions is particularly difficult for organisms such as insects that depend on environmental temperature to regulate their physiological functions. Insects are extremely threatened by global warming, since many do not have enough physiological tolerance even to survive continuous exposure to the current maximum temperatures experienced in their habitats. Here, we review literature on the physiological mechanisms that regulate responses to heat and provide heat tolerance in insects: (i) neuronal mechanisms to detect and respond to heat; (ii) metabolic responses to heat; (iii) thermoregulation; (iv) stress responses to tolerate heat; and (v) hormones that coordinate developmental and behavioural responses at warm temperatures. Our review shows that, apart from the stress response mediated by heat shock proteins, the physiological mechanisms of heat tolerance in insects remain poorly studied. Based on life-history theory, we discuss the costs of heat tolerance and the potential evolutionary mechanisms driving insect adaptations to high temperatures. Some insects may deal with ongoing global warming by the joint action of phenotypic plasticity and genetic adaptation. Plastic responses are limited and may not be by themselves enough to withstand ongoing warming trends. Although the evidence is still scarce and deserves further research in different insect taxa, genetic adaptation to high temperatures may result from rapid evolution. Finally, we emphasize the importance of incorporating physiological information for modelling species distributions and ecological interactions under global warming scenarios. This review identifies several open questions to improve our understanding of how insects respond physiologically to heat and the evolutionary and ecological consequences of those responses. Further lines of research are suggested at the species, order and class levels, with experimental and analytical approaches such as artificial selection, quantitative genetics and comparative analyses.
182 citations
References
More filters
TL;DR: The sensitivity of the commonly used progressive multiple sequence alignment method has been greatly improved and modifications are incorporated into a new program, CLUSTAL W, which is freely available.
Abstract: The sensitivity of the commonly used progressive multiple sequence alignment method has been greatly improved for the alignment of divergent protein sequences. Firstly, individual weights are assigned to each sequence in a partial alignment in order to down-weight near-duplicate sequences and up-weight the most divergent ones. Secondly, amino acid substitution matrices are varied at different alignment stages according to the divergence of the sequences to be aligned. Thirdly, residue-specific gap penalties and locally reduced gap penalties in hydrophilic regions encourage new gaps in potential loop regions rather than regular secondary structure. Fourthly, positions in early alignments where gaps have been opened receive locally reduced gap penalties to encourage the opening up of new gaps at these positions. These modifications are incorporated into a new program, CLUSTAL W which is freely available.
63,427 citations
"Integrating metabolic performance, ..." refers methods in this paper
...Concatenated sequences were aligned using the ClustalW (Thompson et al., 1994) algorithm within MEGA 5....
[...]
...Concatenated sequences were aligned using the ClustalW (Thompson et al., 1994) algorithm within MEGA 5.05 (Tamura et al., 2011)....
[...]
TL;DR: The newest addition in MEGA5 is a collection of maximum likelihood (ML) analyses for inferring evolutionary trees, selecting best-fit substitution models, inferring ancestral states and sequences, and estimating evolutionary rates site-by-site.
Abstract: Comparative analysis of molecular sequence data is essential for reconstructing the evolutionary histories of species and inferring the nature and extent of selective forces shaping the evolution of genes and species. Here, we announce the release of Molecular Evolutionary Genetics Analysis version 5 (MEGA5), which is a user-friendly software for mining online databases, building sequence alignments and phylogenetic trees, and using methods of evolutionary bioinformatics in basic biology, biomedicine, and evolution. The newest addition in MEGA5 is a collection of maximum likelihood (ML) analyses for inferring evolutionary trees, selecting best-fit substitution models (nucleotide or amino acid), inferring ancestral states and sequences (along with probabilities), and estimating evolutionary rates site-by-site. In computer simulation analyses, ML tree inference algorithms in MEGA5 compared favorably with other software packages in terms of computational efficiency and the accuracy of the estimates of phylogenetic trees, substitution parameters, and rate variation among sites. The MEGA user interface has now been enhanced to be activity driven to make it easier for the use of both beginners and experienced scientists. This version of MEGA is intended for the Windows platform, and it has been configured for effective use on Mac OS X and Linux desktops. It is available free of charge from http://www.megasoftware.net.
39,110 citations
"Integrating metabolic performance, ..." refers methods in this paper
...05 (Tamura et al., 2011)....
[...]
...Concatenated sequences were aligned using the ClustalW (Thompson et al., 1994) algorithm within MEGA 5.05 (Tamura et al., 2011)....
[...]
01 Jan 1995
TL;DR: In this paper, the authors present a model for the analysis of variance in a single-classification and two-way and multiway analysis of Variance with the assumption of correlation.
Abstract: 1. Introduction 2. Data in Biology 3. Computers and Data Analysis 4. Descriptive Statistics 5. Introduction to Probability Distributions 6. The Normal Probability Distribution 7. Hypothesis Testing and Interval Estimation 8. Introduction to Analysis of Variance 9. Single-Classification Analysis of Variance 10. Nested Analysis of Variance 11. Two-Way and Multiway Analysis of Variance 12. Statistical Power and Sample Size in the Analysis of Variance 13. Assumptions of Analysis of Variance 14. Linear Regression 15. Correlation 16. Multiple and Curvilinear Regression 17. Analysis of Frequencies 18. Meta-Analysis and Miscellaneous Methods
23,447 citations
Book•
01 Jan 1969
TL;DR: In this paper, the authors present a model for the analysis of variance in a single-classification and two-way and multiway analysis of Variance with the assumption of correlation.
Abstract: 1. Introduction 2. Data in Biology 3. Computers and Data Analysis 4. Descriptive Statistics 5. Introduction to Probability Distributions 6. The Normal Probability Distribution 7. Hypothesis Testing and Interval Estimation 8. Introduction to Analysis of Variance 9. Single-Classification Analysis of Variance 10. Nested Analysis of Variance 11. Two-Way and Multiway Analysis of Variance 12. Statistical Power and Sample Size in the Analysis of Variance 13. Assumptions of Analysis of Variance 14. Linear Regression 15. Correlation 16. Multiple and Curvilinear Regression 17. Analysis of Frequencies 18. Meta-Analysis and Miscellaneous Methods
21,276 citations
TL;DR: A diagnostic fingerprint of temporal and spatial ‘sign-switching’ responses uniquely predicted by twentieth century climate trends is defined and generates ‘very high confidence’ (as laid down by the IPCC) that climate change is already affecting living systems.
Abstract: Causal attribution of recent biological trends to climate change is complicated because non-climatic influences dominate local, short-term biological changes. Any underlying signal from climate change is likely to be revealed by analyses that seek systematic trends across diverse species and geographic regions; however, debates within the Intergovernmental Panel on Climate Change (IPCC) reveal several definitions of a 'systematic trend'. Here, we explore these differences, apply diverse analyses to more than 1,700 species, and show that recent biological trends match climate change predictions. Global meta-analyses documented significant range shifts averaging 6.1 km per decade towards the poles (or metres per decade upward), and significant mean advancement of spring events by 2.3 days per decade. We define a diagnostic fingerprint of temporal and spatial 'sign-switching' responses uniquely predicted by twentieth century climate trends. Among appropriate long-term/large-scale/multi-species data sets, this diagnostic fingerprint was found for 279 species. This suite of analyses generates 'very high confidence' (as laid down by the IPCC) that climate change is already affecting living systems.
9,761 citations
"Integrating metabolic performance, ..." refers background in this paper
...Changes in latitudinal, altitudinal and bathymetric dis- tribution caused by global warming have been increasingly documented across terrestrial and aquatic taxa (e.g., Southward et al., 1995; Menendez & Gutierrez, 1996; Parmesan & Yohe, 2003; Root et al., 2003; Perry et al., 2005)....
[...]