W.C.E.P. Verberk

Delivering on a promise: integrating species traits to transform descriptive community ecology into a predictive science

Abstract. The use of species traits in basic and applied ecology is expanding rapidly because trait-based approaches hold the promise to increase our mechanistic understanding of biological responses. Such understanding could transform descriptive field studies in community ecology into predictive studies. Currently, however, trait-based approaches often fail to reflect species–environment relationships adequately. The difficulties have been perceived mainly as methodological, but we suggest that the problem is more profound and touches on the fundamentals of ecology and evolution. Selection pressures do not act independently on single traits, but rather, on species whose success in a particular environment is controlled by many interacting traits. Therefore, the adaptive value of a particular trait may differ across species, depending on the other traits possessed by the species and the constraints of its body plan. Because of this context-dependence, trait-based approaches should take into account the way combinations of traits interact and are constrained within a species. We present a new framework in which trade-offs and other interactions between biological traits are taken as a starting point from which to develop a better mechanistic understanding of species occurrences. The framework consists of 4 levels: traits, trait interactions, trait combinations, and life-history strategies, in a hierarchy in which each level provides the building blocks for the next. Researchers can contribute knowledge and insights at each level, and their contributions can be verified or falsified using logic, theory, and empirical data. Such an integrated and transparent framework can help fulfill the promise of traits to transform community ecology into a predictive science.

Oxygen supply in aquatic ectotherms: Partial pressure and solubility together explain biodiversity and size patterns

Aquatic ectotherms face the continuous challenge of capturing sufficient oxygen from their environment as the diffusion rate of oxygen in water is 3 x 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 Ficks 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.

Can oxygen set thermal limits in an insect and drive gigantism

Background Thermal limits may arise through a mismatch between oxygen supply and demand in a range of animal taxa. Whilst this oxygen limitation hypothesis is supported by data from a range of marine fish and invertebrates, its generality remains contentious. In particular, it is unclear whether oxygen limitation determines thermal extremes in tracheated arthropods, where oxygen limitation may be unlikely due to the efficiency and plasticity of tracheal systems in supplying oxygen directly to metabolically active tissues. Although terrestrial taxa with open tracheal systems may not be prone to oxygen limitation, species may be affected during other life-history stages, particularly if these rely on diffusion into closed tracheal systems. Furthermore, a central role for oxygen limitation in insects is envisaged within a parallel line of research focussing on insect gigantism in the late Palaeozoic. Methodology/Principal Findings Here we examine thermal maxima in the aquatic life stages of an insect at normoxia, hypoxia (14 kPa) and hyperoxia (36 kPa). We demonstrate that upper thermal limits do indeed respond to external oxygen supply in the aquatic life stages of the stonefly Dinocras cephalotes, suggesting that the critical thermal limits of such aquatic larvae are set by oxygen limitation. This could result from impeded oxygen delivery, or limited oxygen regulatory capacity, both of which have implications for our understanding of the limits to insect body size and how these are influenced by atmospheric oxygen levels. Conclusions/Significance These findings extend the generality of the hypothesis of oxygen limitation of thermal tolerance, suggest that oxygen constraints on body size may be stronger in aquatic environments, and that oxygen toxicity may have actively selected for gigantism in the aquatic stages of Carboniferous arthropods.

Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence

Over the last decade, numerous studies have investigated the role of oxygen in setting thermal tolerance in aquatic animals, and there has been particular focus on arthropods. Arthropods comprise one of the most species-rich taxonomic groups on Earth, and display great diversity in the modes of ventilation, circulation, blood oxygen transport, with representatives living both in water (mainly crustaceans) and on land (mainly insects). The oxygen and capacity limitation of thermal tolerance (OCLTT) hypothesis proposes that the temperature dependent performance curve of animals is shaped by the capacity for oxygen delivery in relation to oxygen demand. If correct, oxygen limitation could provide a mechanistic framework to understand and predict both current and future impacts of rapidly changing climate. In arthropods, most studies testing the OCLTT hypothesis have considered tolerance to thermal extremes. These studies likely operate from the philosophical viewpoint that if the model can predict these critical thermal limits, then it is more likely to also explain loss of performance at less extreme, non-lethal temperatures, for which much less data is available. Nevertheless, the extent to which lethal temperatures are influenced by limitations in oxygen supply remains unresolved. Here we critically evaluate the support and universal applicability for oxygen limitation being involved in lethal temperatures in crustaceans and insects. The relatively few studies investigating the OCLTT hypothesis at low temperature do not support a universal role for oxygen in setting the lower thermal limits in arthropods. With respect to upper thermal limits, the evidence supporting OCLTT is stronger for species relying on underwater gas exchange, while the support for OCLTT in air-breathers is weak. Overall, strongest support was found for increased anaerobic metabolism close to thermal maxima. In contrast, there was only mixed support for the prediction that aerobic scope decreases near critical temperatures, a key feature of the OCLTT hypothesis. In air-breathers, only severe hypoxia (< 2 kPa) affected heat tolerance. The discrepancies for heat tolerance between aquatic and terrestrial organisms can to some extent be reconciled by differences in the capacity to increase oxygen transport. As air-breathing arthropods are unlikely to become oxygen limited under normoxia (especially at rest), the oxygen limitation component in OCLTT does not seem to provide sufficient information to explain lethal temperatures. Nevertheless, many animals may simultaneously face hypoxia and thermal extremes and the combination of these potential stressors is particularly relevant for aquatic organisms where hypoxia (and hyperoxia) is more prevalent. In conclusion, whether taxa show oxygen limitation at thermal extremes may be contingent on their capacity to regulate oxygen uptake, which in turn is linked to their respiratory medium (air vs. water). Fruitful directions for future research include testing multiple predictions of OCLTT in the same species. Additionally, we call for greater research efforts towards studying the role of oxygen in thermal limitation of animal performance at less extreme, sub-lethal temperatures, necessitating studies over longer timescales and evaluating whether oxygen becomes limiting for animals to meet energetic demands associated with feeding, digestion and locomotion.

Respiratory control in aquatic insects dictates their vulnerability to global warming

Forecasting species responses to climatic warming requires knowledge of how temperature impacts may be exacerbated by other environmental stressors, hypoxia being a principal example in aquatic systems. Both stressors could interact directly as temperature affects both oxygen bioavailability and ectotherm oxygen demand. Insufficient oxygen has been shown to limit thermal tolerance in several aquatic ectotherms, although, the generality of this mechanism has been challenged for tracheated arthropods. Comparing species pairs spanning four different insect orders, we demonstrate that oxygen can indeed limit thermal tolerance in tracheates. Species that were poor at regulating oxygen uptake were consistently more vulnerable to the synergistic effects of warming and hypoxia, demonstrating the importance of respiratory control in setting thermal tolerance limits.

Do restoration measures rehabilitate fauna diversity in raised bogs? A comparative study on aquatic macroinvertebrates

To assess whether raised bog restorationmeasures contribute to the conservation andrestoration of the fauna diversity,macroinvertebrate species assemblages werecompared between water bodies created byrewetting measures and water bodies whichhave not been subject to restorationmeasures, but are remnants offormer peat cuttings and trenches used forbuckwheat culture in the past.The restoration sites were inhabited bycharacteristic raised bog species and rarespecies, but their numbers were higher atthe remnant sites not affected byrestoration management. A considerablenumber of characteristic and rare faunaspecies were only found at the remnantsites. The remnant sites includedconsiderably more variation inmacroinvertebrate species assemblages andhad a higher cumulative species richness.The number of characteristicmacroinvertebrate species was not clearlyrelated to the presence of a characteristicraised bog vegetation. In restoration sitesnumbers of rare and characteristic speciesper site tended to increase with the timeelapsed after rewetting. However,restoration measures will not automaticallyresult in restoration of a more or lesscomplete macroinvertebrate speciesspectrum, as restoration measures have sofar resulted in habitats for only a limitednumber of the characteristic species.When planning restoration measures, it isrecommended to protect the populations ofrare and characteristic species present inthe area, as these populations may becomethe sources for colonization of rewettedsites. Safeguarding habitat diversityduring the restoration process andrestoration of different elements of thehabitat diversity of complete raised bogsystems will result in the characteristicfauna diversity being conserved andrestored more successfully.

Why polar gigantism and palaeozoic gigantism are not equivalent: Effects of oxygen and temperature on the body size of ectotherms

Summary 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.

Anaerobic Metabolism at Thermal Extremes: A Metabolomic Test of the Oxygen Limitation Hypothesis in an Aquatic Insect

Thermal limits in ectotherms may arise through a mismatch between supply and demand of oxygen. At higher temperatures, the ability of their cardiac and ventilatory activities to supply oxygen becomes insufficient to meet their elevated oxygen demand. Consequently, higher levels of oxygen in the environment are predicted to enhance tolerance of heat, whereas reductions in oxygen are expected to reduce thermal limits. Here, we extend previous research on thermal limits and oxygen limitation in aquatic insect larvae and directly test the hypothesis of increased anaerobic metabolism and lower energy status at thermal extremes. We quantified metabolite profiles in stonefly nymphs under varying temperatures and oxygen levels. Under normoxia, the concept of oxygen limitation applies to the insects studied. Shifts in the metabolome of heat-stressed stonefly nymphs clearly indicate the onset of anaerobic metabolism (e.g., accumulation of lactate, acetate, and alanine), a perturbation of the tricarboxylic acid cycle (e.g., accumulation of succinate and malate), and a decrease in energy status (e.g., ATP), with corresponding decreases in their ability to survive heat stress. These shifts were more pronounced under hypoxic conditions, and negated by hyperoxia, which also improved heat tolerance. Perturbations of metabolic pathways in response to either heat stress or hypoxia were found to be somewhat similar but not identical. Under hypoxia, energy status was greatly compromised at thermal extremes, but energy shortage and anaerobic metabolism could not be conclusively identified as the sole cause underlying thermal limits under hyperoxia. Metabolomics proved useful for suggesting a range of possible mechanisms to explore in future investigations, such as the involvement of leaking membranes or free radicals. In doing so, metabolomics provided a more complete picture of changes in metabolism under hypoxia and heat stress.

Field and laboratory studies reveal interacting effects of stream oxygenation and warming on aquatic ectotherms

Abstract Aquatic ecological responses to climatic warming are complicated by interactions between thermal effects and other environmental stressors such as organic pollution and hypoxia. Laboratory experiments have demonstrated how oxygen limitation can set heat tolerance for some aquatic ectotherms, but only at unrealistic lethal temperatures and without field data to assess whether oxygen shortages might also underlie sublethal warming effects. Here, we test whether oxygen availability affects both lethal and nonlethal impacts of warming on two widespread Eurasian mayflies, Ephemera danica, Müller 1764 and Serratella ignita (Poda 1761). Mayfly nymphs are often a dominant component of the invertebrate assemblage in streams, and play a vital role in aquatic and riparian food webs. In the laboratory, lethal impacts of warming were assessed under three oxygen conditions. In the field, effects of oxygen availability on nonlethal impacts of warming were assessed from mayfly occurrence in 42 293 UK stream samples where water temperature and biochemical oxygen demand were measured. Oxygen limitation affected both lethal and sublethal impacts of warming in each species. Hypoxia lowered lethal limits by 5.5 °C (±2.13) and 8.2 °C (±0.62) for E. danica and S. ignita respectively. Field data confirmed the importance of oxygen limitation in warmer waters; poor oxygenation drastically reduced site occupancy, and reductions were especially pronounced under warm water conditions. Consequently, poor oxygenation lowered optimal stream temperatures for both species. The broad concordance shown here between laboratory results and extensive field data suggests that oxygen limitation not only impairs survival at thermal extremes but also restricts species abundance in the field at temperatures well below upper lethal limits. Stream oxygenation could thus control the vulnerability of aquatic ectotherms to global warming. Improving water oxygenation and reducing pollution can provide key facets of climate change adaptation for running waters.

Biological traits successfully predict the effects of restoration management on macroinvertebrates in shallow softwater lakes

Many shallow softwater lakes are being affected by eutrophication and acidification. In these small lakes decaying organic material usually accumulates and characteristic plant and animal species disappear. In many degraded lakes organic matter and macrophytes are being removed in order to restore the lakes to their original state. To assess the effects of restoration management in softwater lakes on aquatic macroinvertebrates, changes in the species assemblages were studied in four degraded lakes in the Netherlands undergoing restoration measures. The degraded lakes still harboured species characteristic of pristine softwaters. However, most of these species were not recorded after restoration measures were taken. Species’ densities declined dramatically during the execution of restoration measures. Swimming and abundant species were more likely to survive the restoration measures than other species. The first years after restoration, the lakes did not meet the habitat requirements for a number of species. Species requiring vegetation for ovipositioning, animal food sources and swards of vegetation as habitat declined. Because recolonization is expected to be restricted, it is recommended to ensure the survival of relict populations when taking measures to restore degraded softwater lakes. This may be achieved by phasing restoration measures in space and time, hereby minimizing mortality during the execution of restoration measures and by preserving habitat conditions required by characteristic species.