Patterns in physiological trait variation delineate potential impacts of climate change on ectotherms

Pintor, Anna Francisca Valentina (2015) Patterns in physiological trait variation delineate potential impacts of climate change on ectotherms. PhD thesis, James Cook University.

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Abstract

Understanding the physiological and behavioural mechanisms that limit species' distributions is essential to our understanding of species' evolutionary physiology, as well as our ability to predict differential impacts of climate change. Despite the re-emerging interest in physiological determinants of large-scale biogeographic patterns (macrophysiology), substantial knowledge gaps remain in our understanding of the drivers of differential evolution of physiological traits and the potential for these traits to limit species' ability to cope with climatic extremes. Ectotherms are of particular concern, because they make up most of the world's biodiversity (invertebrates, fish, amphibians, reptiles, and plants) and are highly susceptible to spatial and temporal variation in thermal regimes. Problems in the relevant literature include;

(i) Focus on the presence or absence of biogeographic patterns rather than their underlying mechanisms,

(ii) Inadequate or inconsistent, assessment of phenotypic plasticity (acclimation potential) across studies used for meta-analyses,

(iii) Limited knowledge on how behaviour modifies exposure to extremes,

(iv) Under-appreciation of desiccation risk as a limiting factor in addition to thermal constraints,

(v) Lack of studies on comprehensive sets of thermal traits within a phylogenetically and methodologically controlled frame work, and

(vi) Lack of knowledge on which, of the many, traits affected by temperature are physiologically and geographically the most limiting to ectothermic organisms.

In Chapter I, I use published data to review the validity of one of the most heavily debated biogeographic pattern, Rapoport's Rule, and its underlying mechanism, the Climatic Variability Hypothesis. I provide a novel approach to testing the Climatic Variability Hypothesis and show that it applies even to taxa that do not follow the pattern of Rapoport's Rule.

In Chapter II, I describe the complete acclimation process of critical thermal minimum temperatures in tropical ectotherms to establish the length and extent of this process and assess the degree to which previous studies may underestimate thermal tolerances because of inconsistent, short acclimation times. I show that acclimation of lower thermal limits, which contribute substantially to estimates of thermal tolerance breadth, can take more than 16 weeks to complete, even in a tropical ectotherm with little natural exposure to cold conditions. Current estimates of thermal tolerance based on inconsistent, partial acclimation, consequently greatly bias our estimates of thermal tolerances.

Chapter III examines how behavioural hydroregulation reduces exposure of "dry-skinned" ectotherms to conditions that promote high desiccation rates. Active hydroregulation is present in dry-skinned ectotherms from tropical rainforests and desiccation avoidance clashes with thermoregulation, placing individuals in thermally suboptimal conditions and likely reducing activity times in dry conditions.

In Chapter IV, I provide a comprehensive study of inter- and intraspecific variation in fully acclimated thermal traits in a clade of small, dry-skinned ectotherms from Eastern Australia across a natural geographic gradient. Water loss rates, metabolic rates, critical thermal minima, thermoregulatory behaviour and performance parameters vary along the latitudinal gradient in temperature. However, upper thermal limits, although often used to predict vulnerability of tropical and temperate organisms to climate change, do not vary with latitude.

Chapter V assesses interactions between thermoregulatory behaviour and thermal dependence of performance to establish how the former may buffer exposure to extremes. The combined effects of behavioural hydroregulation and thermoregulation may buffer species against environmental variability and enable them to occur in conditions far outside their physiological tolerance limits. While decreasing risk of overheating and desiccation, these behaviours may, however, greatly limit potential activity time and, therefore, fitness. Vulnerability of ectotherms to increasing temperatures may be determined by increases desiccation, as well as by impacts of reduced activity times and increased metabolic expenditure on species' energy budgets, rather than simply by risk of overheating. Substantial intraspecific variation in metabolic rate and lower thermal limit suggests strong selection pressures on these traits.

Chapter VI considers which physiological or behavioural traits best predict species' potential to extend into climatic extremes. Metabolic compensation to cold and cold tolerance are the best predictors of species' potential to extend into colder regions, while physiological heat tolerance is not a significant predictor of mean or maximum air temperatures species extend into, but rather appears to predict tolerance to high radiation levels. Overheating is, therefore, likely to affect ectotherms through species' capacity to deal with high levels or frequency of exposure to radiation, rather than high ambient air temperatures. Water loss rates are a significant predictor of species' potential to extend into dry habitats, even in dry-skinned ectotherms, and are underappreciated in their relevance for species' vulnerability to climate change, which is predicted to not only increase temperatures, but also moisture deficit and frequency of drought.

Future studies should assess variation in desiccation resistance across geographically and taxonomically broader scales to enhance our ability to predict impacts of climate change. This study provides fine-scale, novel insight into determinants of limits to species' current and future distribution and is the most comprehensive analysis of thermal trait variation in a taxon to date.

Item ID: 46269
Item Type: Thesis (PhD)
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Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter I: Pintor, Anna F.V., Schwarzkopf, Lin, and Krockenberger, Andrew K. (2015) Rapoport's Rule: do climatic variability gradients shape range extent? Ecological Monographs, 85 (4). pp. 643-659.

Chapter II: Pintor, Anna F.V., Schwarzkopf, Lin, and Krockenberger, Andrew K. (2016) Extensive Acclimation in Ectotherms Conceals Interspecific Variation in Thermal Tolerance Limits. PLoS ONE, 11 (3). pp. 1-15.

Chapter III: Pintor, Anna F.V., Schwarzkopf, Lin, and Krockenberger, Andrew K. (2016) Hydroregulation in a tropical dry-skinned ectotherm. Oecologia, 182 (4). pp. 925-931.

Research Data: http://dx.doi.org/10.4225/28/5536F28D28A5E, http://dx.doi.org/10.4225/28/55B58FDB5613E, http://dx.doi.org/10.4225/28/55B58C5D690A8, http://dx.doi.org/10.4225/28/55B59232DCAF4, http://dx.doi.org/10.4225/28/55B58E6C46947
Date Deposited: 08 Nov 2016 01:26
FoR Codes: 06 BIOLOGICAL SCIENCES > 0606 Physiology > 060604 Comparative Physiology @ 33%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060806 Animal Physiological Ecology @ 34%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060302 Biogeography and Phylogeography @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 50%
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