ABSTRACT
Body size is central to ecology at levels ranging from organismal fecundity to the functioning of communities and ecosystems. Understanding temperature‐induced variations in body size is ...therefore of fundamental and applied interest, yet thermal responses of body size remain poorly understood. Temperature–size (T–S) responses tend to be negative (e.g. smaller body size at maturity when reared under warmer conditions), which has been termed the temperature–size rule (TSR). Explanations emphasize either physiological mechanisms (e.g. limitation of oxygen or other resources and temperature‐dependent resource allocation) or the adaptive value of either a large body size (e.g. to increase fecundity) or a short development time (e.g. in response to increased mortality in warm conditions). Oxygen limitation could act as a proximate factor, but we suggest it more likely constitutes a selective pressure to reduce body size in the warm: risks of oxygen limitation will be reduced as a consequence of evolution eliminating genotypes more prone to oxygen limitation. Thus, T–S responses can be explained by the ‘Ghost of Oxygen‐limitation Past’, whereby the resulting (evolved) T–S responses safeguard sufficient oxygen provisioning under warmer conditions, reflecting the balance between oxygen supply and demands experienced by ancestors. T–S responses vary considerably across species, but some of this variation is predictable. Body‐size reductions with warming are stronger in aquatic taxa than in terrestrial taxa. We discuss whether larger aquatic taxa may especially face greater risks of oxygen limitation as they grow, which may be manifested at the cellular level, the level of the gills and the whole‐organism level. In contrast to aquatic species, terrestrial ectotherms may be less prone to oxygen limitation and prioritize early maturity over large size, likely because overwintering is more challenging, with concomitant stronger end‐of season time constraints. Mechanisms related to time constraints and oxygen limitation are not mutually exclusive explanations for the TSR. Rather, these and other mechanisms may operate in tandem. But their relative importance may vary depending on the ecology and physiology of the species in question, explaining not only the general tendency of negative T–S responses but also variation in T–S responses among animals differing in mode of respiration (e.g. water breathers versus air breathers), genome size, voltinism and thermally associated behaviour (e.g. heliotherms).
Aquatic ectotherms face the continuous challenge of capturing sufficient oxygen from their environment as the diffusion rate of oxygen in water is 3 ×× 10
5
times lower than in air. Despite the ...recognized importance of oxygen in shaping aquatic communities, consensus on what drives environmental oxygen availability is lacking. Physiologists emphasize oxygen partial pressure, while ecologists emphasize oxygen solubility, traditionally expressing oxygen in terms of concentrations. To resolve the question of whether partial pressure or solubility limits oxygen supply in nature, we return to first principles and derive an index of oxygen supply from Fick's classic first law of diffusion. This oxygen supply index (OSI) incorporates both partial pressure and solubility. Our OSI successfully explains published patterns in body size and species across environmental clines linked to differences in oxygen partial pressure (altitude, organic pollution) or oxygen solubility (temperature and salinity). Moreover, the OSI was more accurately and consistently related to these ecological patterns than other measures of oxygen (oxygen saturation, dissolved oxygen concentration, biochemical oxygen demand concentrations) and similarly outperformed temperature and altitude, which covaried with these environmental clines. Intriguingly, by incorporating gas diffusion rates, it becomes clear that actually more oxygen is available to an organism in warmer habitats where lower oxygen concentrations would suggest the reverse. Under our model, the observed reductions in aerobic performance in warmer habitats do not arise from lower oxygen concentrations, but instead through organismal oxygen demand exceeding supply. This reappraisal of how organismal thermal physiology and oxygen demands together shape aerobic performance in aquatic ectotherms and the new insight of how these components change with temperature have broad implications for predicting the responses of aquatic communities to ongoing global climate shifts.
1. A positive interspecific abundance-occupancy relationship is one of the most robust patterns in macroecology. Yet, the mechanisms driving this pattern are poorly understood. Here, we use ...biological traits of freshwater macroinvertebrates to gain a mechanistic understanding and disentangle the various explanations. We ask whether mechanisms underlying the abundance-occupancy relationship differ between species, and whether information on individual species can be used to explain their contribution to the interspecific relationship. 2. We test the hypothesis that the importance of metapopulation dynamics or niche differences in explaining the relationship differs between species, varying in relation to their habitat breadth. In addition, we analyse how a species' biological traits shape its habitat breadth and its abundance and occupancy. 3. The abundance and occupancy of the 234 different aquatic macroinvertebrate species were strongly and positively related. Marked differences were found between habitat specialists and habitat generalists in the goodness-of-fit of abundance-occupancy relationships. The occupancy-frequency distribution was bimodal for habitat generalists, allowing 'satellite species' to be distinguished from 'core species'. 4. Habitat generalists appeared to be more widespread but less abundant than habitat specialists, suggesting that the jack-of-all-trades may be master-of-none. Species traits (trophic position and other life-history traits) explained a significant part of the variation around the general relationship. Among habitat specialists, more species showed synchronized life cycles, a low dispersal capacity or clustered oviposition, being better adapted to predictable habitats. Among habitat generalists, more species had long-lived adults, spreading reproductive effort in time and space, and were strong dispersers, being better adapted to unpredictable habitats. 5. Interspecific abundance-occupancy relationships can be best understood by examining the contribution of individual species. For habitat specialists, the interplay between niche differences (diet and habitat use) and the underlying spatial distribution of environmental conditions result in competitive displacement and differences in species' success. For habitat generalists, differences in colonization and extinction rates between species are more important. Therefore, both metapopulation dynamics and niche differences can operate simultaneously but apply to different species, thus constituting different endpoints of the same continuum.
Insects can experience functional hypoxia, a situation in which O
2
supply is inadequate to meet oxygen demand. Assessing when functional hypoxia occurs is complex, because responses are graded, age ...and tissue dependent, and compensatory. Here, we compare information gained from metabolomics and transcriptional approaches and by manipulation of the partial pressure of oxygen. Functional hypoxia produces graded damage, including damaged macromolecules and inflammation. Insects respond by compensatory physiological and morphological changes in the tracheal system, metabolic reorganization, and suppression of activity, feeding, and growth. There is evidence for functional hypoxia in eggs, near the end of juvenile instars, and during molting. Functional hypoxia is more likely in species with lower O
2
availability or transport capacities and when O
2
need is great. Functional hypoxia occurs normally during insect development and is a factor in mediating life-history trade-offs.
Organisms of gigantic proportions inhabited the world at a time of a hyperoxic prehistoric atmosphere (Palaeozoic gigantism). Extant giants are found in cold polar waters, with large quantities of ...dissolved oxygen (polar gigantism). Oxygen is usually deemed central to explain such gigantism. Examples of one category of gigantism are often cited in support of the other, but novel insights into the bioavailability of oxygen imply that they cannot be taken as equivalent manifestations of the effect of oxygen on body size. Recently, the availability of oxygen has been shown to be lower in cold waters, despite greater oxygen solubility. Consequently, gigantism in cold, oxygenated waters and gigantism in an oxygen‐pressurized world are fundamentally different: Palaeozoic gigantism likely arose because of greater oxygen availability, while polar gigantism arises in spite of lower oxygen availability. The traditional view of respiration focuses on meeting the challenge of extracting sufficient amounts of oxygen, which essentially is a toxic gas. We present a broader perspective, which specifically includes risks of oxygen poisoning. We discuss how challenges pertaining to balancing oxygen uptake capacity and risks of oxygen poisoning are very different for animals breathing either air or water. We propose a novel explanation for polar gigantism in aquatic ectotherms, arguing that their larger body size represents a respiratory advantage that helps to overcome the larger viscous forces in water. Being large helps organisms to balance the opposing risks of asphyxiation and poisoning, especially in colder, more viscous, water. This results in a selection for larger sizes, with polar gigantism as the extreme manifestation. Hence, a larger size provides respiratory benefits to water‐breathing ectotherms, but not terrestrial ectotherms. This can explain why clines in body size across temperature and latitude are stronger in aquatic ectotherms.
Thermal tolerance patterns across latitude and elevation Sunday, Jennifer; Bennett, Joanne M; Calosi, Piero ...
Philosophical transactions - Royal Society. Biological sciences,
08/2019, Letnik:
374, Številka:
1778
Journal Article
Recenzirano
Odprti dostop
Linking variation in species' traits to large-scale environmental gradients can lend insight into the evolutionary processes that have shaped functional diversity and future responses to ...environmental change. Here, we ask how heat and cold tolerance vary as a function of latitude, elevation and climate extremes, using an extensive global dataset of ectotherm and endotherm thermal tolerance limits, while accounting for methodological variation in acclimation temperature, ramping rate and duration of exposure among studies. We show that previously reported relationships between thermal limits and latitude in ectotherms are robust to variation in methods. Heat tolerance of terrestrial ectotherms declined marginally towards higher latitudes and did not vary with elevation, whereas heat tolerance of freshwater and marine ectotherms declined more steeply with latitude. By contrast, cold tolerance limits declined steeply with latitude in marine, intertidal, freshwater and terrestrial ectotherms, and towards higher elevations on land. In all realms, both upper and lower thermal tolerance limits increased with extreme daily temperature, suggesting that different experienced climate extremes across realms explain the patterns, as predicted under the Climate Extremes Hypothesis. Statistically accounting for methodological variation in acclimation temperature, ramping rate and exposure duration improved model fits, and increased slopes with extreme ambient temperature. Our results suggest that fundamentally different patterns of thermal limits found among the earth's realms may be largely explained by differences in episodic thermal extremes among realms, updating global macrophysiological 'rules'. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.
Aerobic metabolism generates 15–20 times more energy (ATP) than anaerobic metabolism, which is crucial in maintaining energy budgets in animals, fueling metabolism, activity, growth and reproduction. ...For ectothermic water‐breathers such as fishes, low dissolved oxygen may limit oxygen uptake and hence aerobic metabolism. Here, we assess, within a phylogenetic context, how abiotic and biotic drivers explain the variation in hypoxia tolerance observed in fishes. To do so, we assembled a database of hypoxia tolerance, measured as critical oxygen tensions (Pcrit) for 195 fish species. Overall, we found that hypoxia tolerance has a clear phylogenetic signal and is further modulated by temperature, body mass, cell size, salinity and metabolic rate. Marine fishes were more susceptible to hypoxia than freshwater fishes. This pattern is consistent with greater fluctuations in oxygen and temperature in freshwater habitats. Fishes with higher oxygen requirements (e.g. a high metabolic rate relative to body mass) also were more susceptible to hypoxia. We also found evidence that hypoxia and warming can act synergistically, as hypoxia tolerance was generally lower in warmer waters. However, we found significant interactions between temperature and the body and cell size of a fish. Constraints in oxygen uptake related to cellular surface area to volume ratios and effects of viscosity on the thickness of the boundary layers enveloping the gills could explain these thermal dependencies. The lower hypoxia tolerance in warmer waters was particularly pronounced for fishes with larger bodies and larger cell sizes. Previous studies have found a wide diversity in the direction and strength of relationships between Pcrit and body mass. By including interactions with temperature, our study may help resolve these divergent findings, explaining the size dependency of hypoxia tolerance in fish.
Whether fish can tolerate low levels of dissolved oxygen is shown here to depend on characteristics of both the fish (body mass, genome size and metabolism) and the water (temperature and salinity). These effects did not act in isolation: In warmer waters, small fishes with small genomes were more tolerant than large fishes with large genomes. We also observed a greater tolerance in freshwater fishes, compared to marine fishes. These findings can help to (i) resolve the scientific debate about oxygen limitation and (ii) predict the impacts of climate change on global fish populations and fisheries.
Forecasting long‐term consequences of global warming requires knowledge on thermal mortality and how heat stress interacts with other environmental stressors on different timescales. Here, we ...describe a flexible analytical framework to forecast mortality risks by combining laboratory measurements on tolerance and field temperature records. Our framework incorporates physiological acclimation effects, temporal scale differences and the ecological reality of fluctuations in temperature, and other factors such as oxygen. As a proof of concept, we investigated the heat tolerance of amphipods Dikerogammarus villosus and Echinogammarus trichiatus in the river Waal, the Netherlands. These organisms were acclimated to different temperatures and oxygen levels. By integrating experimental data with high‐resolution field data, we derived the daily heat mortality probabilities for each species under different oxygen levels, considering current temperatures as well as 1 and 2°C warming scenarios. By expressing heat stress as a mortality probability rather than a upper critical temperature, these can be used to calculate cumulative annual mortality, allowing the scaling up from individuals to populations. Our findings indicate a substantial increase in annual mortality over the coming decades, driven by projected increases in summer temperatures. Thermal acclimation and adequate oxygenation improved heat tolerance and their effects were magnified on longer timescales. Consequently, acclimation effects appear to be more effective than previously recognized and crucial for persistence under current temperatures. However, even in the best‐case scenario, mortality of D. villosus is expected to approach 100% by 2100, while E. trichiatus appears to be less vulnerable with mortality increasing to 60%. Similarly, mortality risks vary spatially: In southern, warmer rivers, riverine animals will need to shift from the main channel toward the cooler head waters to avoid thermal mortality. Overall, this framework generates high‐resolution forecasts on how rising temperatures, in combination with other environmental stressors such as hypoxia, impact ecological communities.
We describe a flexible analytical framework to forecast heat mortality in riverine amphipods, incorporating physiological acclimation, temporal scale and differences in water oxygenation. We bridge the gap between experimental data and the ecological reality of thermal fluctuations by expressing heat tolerance as mortality probabilities and accumulating these over time. Our findings indicate that thermal acclimation and adequate oxygenation improved heat tolerance and these improvements were more pronounced on longer timescales. Consequently, acclimation effects were more effective than previously recognized and crucial for amphipod persistence. Our framework provides spatial and temporal forecasts, illustrating how warming and hypoxia will impact ecological communities.
Both oxygen and temperature are fundamental factors determining metabolic performance, fitness, ecological niches, and responses of many aquatic organisms to climate change. Despite the importance of ...physical and physiological constraints on oxygen supply affecting aerobic metabolism of aquatic ectotherms, ecological theories such as the metabolic theory of ecology have focused on the effects of temperature rather than oxygen. This gap currently impedes mechanistic models from accurately predicting metabolic rates (i.e., oxygen consumption rates) of aquatic organisms and restricts predictions to resting metabolism, which is less affected by oxygen limitation. Here, we expand on models of metabolic scaling by accounting for the role of oxygen availability and temperature on both resting and active metabolic rates. Our model predicts that oxygen limitation is more likely to constrain metabolism in larger, warmer, and active fish. Consequently, active metabolic rates are less responsive to temperature than are resting metabolic rates, and metabolism scales to body size with a smaller exponent whenever temperatures or activity levels are higher. Results from a metaanalysis of fish metabolic rates are consistent with our model predictions. The observed interactive effects of temperature, oxygen availability, and body size predict that global warming will limit the aerobic scope of aquatic ectotherms and may place a greater metabolic burden on larger individuals, impairing their physiological performance in the future. Our model reconciles the metabolic theory with empirical observations of oxygen limitation and provides a formal, quantitative framework for predicting both resting and active metabolic rate and hence aerobic scope of aquatic ectotherms.
In order to predict which species can successfully cope with global warming and how other environmental stressors modulate their vulnerability to climate‐related environmental factors, an ...understanding of the ecophysiology underpinning thermal limits is essential for both conservation biology and invasion biology.
Heat tolerance and the extent to which heat tolerance differed with oxygen availability were examined for four native and four alien freshwater peracarid crustacean species, with differences in habitat use across species. Three hypotheses were tested: (1) Heat and lack of oxygen synergistically reduce survival of species; (2) patterns in heat tolerance and the modulation thereof by oxygen differ between alien and native species and between species with different habitat use; (3) small animals can better tolerate heat than large animals, and this difference is more pronounced under hypoxia.
To assess heat tolerances under different oxygen levels, animal survival was monitored in experimental chambers in which the water temperature was ramped up (0.25°C min−1). Heat tolerance (CTmax) was scored as the cessation of all pleopod movement, and heating trials were performed under hypoxia (5 kPa oxygen), normoxia (20 kPa) and hyperoxia (60 kPa).
Heat tolerance differed across species as did the extent by which heat tolerance was affected by oxygen conditions. Heat‐tolerant species, for example, Asellus aquaticus and Crangonyx pseudogracilis, showed little response to oxygen conditions in their CTmax, whereas the CTmax of heat‐sensitive species, for example, Dikerogammarus villosus and Gammarus fossarum, was more plastic, being increased by hyperoxia and reduced by hypoxia.
In contrast to other studies on crustaceans, alien species were not more heat‐tolerant than native species. Instead, differences in heat tolerance were best explained by habitat use, with species from standing waters being heat tolerant and species from running waters being heat sensitive. In addition, larger animals displayed lower critical maximum temperature, but only under hypoxia. An analysis of data available in the literature on metabolic responses of the study species to temperature and oxygen conditions suggests that oxygen conformers and species whose oxygen demand rapidly increases with temperature (low activation energy) may be more heat sensitive.
The alien species D. villosus appeared most susceptible to hypoxia and heat stress. This may explain why this species is very successful in colonizing new areas in littoral zones with rocky substrate which are well aerated due to continuous wave action generated by passing ships or prevailing winds. This species is less capable of spreading to other waters which are poorly oxygenated and where C. pseudogracilis is the more likely dominant alien species.
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