Publications by authors named "Wilco C E P Verberk"

32 Publications

Do aquatic ectotherms perform better under hypoxia after warm acclimation?

J Exp Biol 2021 02 4;224(Pt 3). Epub 2021 Feb 4.

Marine Biology and Ecology Research Centre, Plymouth University, Drake Circus, PL4 8AA, UK.

Aquatic animals increasingly encounter environmental hypoxia due to climate-related warming and/or eutrophication. Although acute warming typically reduces performance under hypoxia, the ability of organisms to modulate hypoxic performance via thermal acclimation is less understood. Here, we review the literature and ask whether hypoxic performance of aquatic ectotherms improves following warm acclimation. Interpretation of thermal acclimation effects is limited by reliance on data from experiments that are not designed to directly test for beneficial or detrimental effects on hypoxic performance. Most studies have tested hypoxic responses exclusively at test temperatures matching organisms' acclimation temperatures, precluding the possibility of distinguishing between acclimation and acute thermal effects. Only a few studies have applied appropriate methodology to identify beneficial thermal acclimation effects on hypoxic performance, i.e. acclimation to different temperatures prior to determining hypoxic responses at standardised test temperatures. These studies reveal that acute warming predominantly impairs hypoxic performance, whereas warm acclimation tends to be either beneficial or have no effect. If this generalises, we predict that warm-acclimated individuals in some species should outperform non-acclimated individuals under hypoxia. However, acclimation seems to only partially offset acute warming effects; therefore, aquatic ectotherms will probably display overall reduced hypoxic performance in the long term. Drawing on the appropriate methodology, future studies can quantify the ability of organisms to modulate hypoxic performance via (reversible) thermal acclimation and unravel the underlying mechanisms. Testing whether developmental acclimation and multigenerational effects allow for a more complete compensation is essential to allow us to predict species' resilience to chronically warmer, hypoxic environments.
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http://dx.doi.org/10.1242/jeb.232512DOI Listing
February 2021

Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms.

Proc Natl Acad Sci U S A 2020 12 30;117(50):31963-31968. Epub 2020 Nov 30.

Division of Biological Sciences, University of Montana, Missoula, MT 59812.

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.
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http://dx.doi.org/10.1073/pnas.2003292117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7749359PMC
December 2020

Are acute and acclimated thermal effects on metabolic rate modulated by cell size? A comparison between diploid and triploid zebrafish larvae.

J Exp Biol 2021 01 11;224(Pt 1). Epub 2021 Jan 11.

Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, 6525 AJ Nijmegen, The Netherlands.

Being composed of small cells may carry energetic costs related to maintaining ionic gradients across cell membranes as well as benefits related to diffusive oxygen uptake. Here, we test the hypothesis that these costs and benefits of cell size in ectotherms are temperature dependent. To study the consequences of cell size for whole-organism metabolic rate, we compared diploid and triploid zebrafish larvae differing in cell size. A fully factorial design was applied combining three different rearing and test temperatures that allowed us to distinguish acute from acclimated thermal effects. Individual oxygen consumption rates of diploid and triploid larvae across declining levels of oxygen availability were measured. We found that both acute and acclimated thermal effects affected the metabolic response. In comparison with triploids, diploids responded more strongly to acute temperatures, especially when reared at the highest temperature. These observations support the hypothesis that animals composed of smaller cells (i.e. diploids) are less vulnerable to oxygen limitation in warm aquatic habitats. Furthermore, we found slightly improved hypoxia tolerance in diploids. By contrast, warm-reared triploids had higher metabolic rates when they were tested at acute cold temperature, suggesting that being composed of larger cells may provide metabolic advantages in the cold. We offer two mechanisms as a potential explanation of this result, related to homeoviscous adaptation of membrane function and the mitigation of developmental noise. Our results suggest that being composed of larger cells provides metabolic advantages in cold water, while being composed of smaller cells provides metabolic advantages in warm water.
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http://dx.doi.org/10.1242/jeb.227124DOI Listing
January 2021

Shrinking body sizes in response to warming: explanations for the temperature-size rule with special emphasis on the role of oxygen.

Biol Rev Camb Philos Soc 2021 02 22;96(1):247-268. Epub 2020 Sep 22.

Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands.

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).
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http://dx.doi.org/10.1111/brv.12653DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7821163PMC
February 2021

Trait-based ecology at large scales: Assessing functional trait correlations, phylogenetic constraints and spatial variability using open data.

Glob Chang Biol 2020 Dec 18;26(12):7255-7267. Epub 2020 Oct 18.

School of Geography/[email protected], University of Leeds, Leeds, UK.

The growing use of functional traits in ecological research has brought new insights into biodiversity responses to global environmental change. However, further progress depends on overcoming three major challenges involving (a) statistical correlations between traits, (b) phylogenetic constraints on the combination of traits possessed by any single species, and (c) spatial effects on trait structure and trait-environment relationships. Here, we introduce a new framework for quantifying trait correlations, phylogenetic constraints and spatial variability at large scales by combining openly available species' trait, occurrence and phylogenetic data with gridded, high-resolution environmental layers and computational modelling. Our approach is suitable for use among a wide range of taxonomic groups inhabiting terrestrial, marine and freshwater habitats. We demonstrate its application using freshwater macroinvertebrate data from 35 countries in Europe. We identified a subset of available macroinvertebrate traits, corresponding to a life-history model with axes of resistance, resilience and resource use, as relatively unaffected by correlations and phylogenetic constraints. Trait structure responded more consistently to environmental variation than taxonomic structure, regardless of location. A re-analysis of existing data on macroinvertebrate communities of European alpine streams supported this conclusion, and demonstrated that occurrence-based functional diversity indices are highly sensitive to the traits included in their calculation. Overall, our findings suggest that the search for quantitative trait-environment relationships using single traits or simple combinations of multiple traits is unlikely to be productive. Instead, there is a need to embrace the value of conceptual frameworks linking community responses to environmental change via traits which correspond to the axes of life-history models. Through a novel integration of tools and databases, our flexible framework can address this need.
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http://dx.doi.org/10.1111/gcb.15344DOI Listing
December 2020

Universal metabolic constraints shape the evolutionary ecology of diving in animals.

Proc Biol Sci 2020 05 27;287(1927):20200488. Epub 2020 May 27.

Marine Biology and Ecology Research Centre, School of Biological and Marine Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK.

Diving as a lifestyle has evolved on multiple occasions when air-breathing terrestrial animals invaded the aquatic realm, and diving performance shapes the ecology and behaviour of all air-breathing aquatic taxa, from small insects to great whales. Using the largest dataset yet assembled, we show that maximum dive duration increases predictably with body mass in both ectotherms and endotherms. Compared to endotherms, ectotherms can remain submerged for longer, but the mass scaling relationship for dive duration is much steeper in endotherms than in ectotherms. These differences in diving allometry can be fully explained by inherent differences between the two groups in their metabolic rate and how metabolism scales with body mass and temperature. Therefore, we suggest that similar constraints on oxygen storage and usage have shaped the evolutionary ecology of diving in all air-breathing animals, irrespective of their evolutionary history and metabolic mode. The steeper scaling relationship between body mass and dive duration in endotherms not only helps explain why the largest extant vertebrate divers are endothermic rather than ectothermic, but also fits well with the emerging consensus that large extinct tetrapod divers (e.g. plesiosaurs, ichthyosaurs and mosasaurs) were endothermic.
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http://dx.doi.org/10.1098/rspb.2020.0488DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7287373PMC
May 2020

Changes in heat stress tolerance in a freshwater amphipod following starvation: The role of oxygen availability, metabolic rate, heat shock proteins and energy reserves.

Comp Biochem Physiol A Mol Integr Physiol 2020 07 1;245:110697. Epub 2020 Apr 1.

Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010, 6500 GL, Heyendaalseweg 135, 6525, AJ, Nijmegen, the Netherlands. Electronic address:

The ability of organisms to cope with environmental stressors depends on the duration and intensity of the stressor, as well as the type of stress. For aquatic organisms, oxygen limitation has been implicated in limiting heat tolerance. Here we examine how starvation affects heat tolerance in the amphipod Gammarus fossarum (Koch, 1836) and whether observed changes can be explained from alterations in oxidative metabolism, depletion of energy reserves, upregulation of heat shock proteins or susceptibility to oxygen limitation. Starved amphipods showed impaired survival compared to fed amphipods during prolonged exposure to mild heat. In contrast, under acute, high-intensity heat exposure they actually showed improved survival. We observed a lower demand for oxygen in starved amphipods which could make them less susceptible to oxygen limitation. Such a role for oxygen in limiting heat tolerance was verified as hypoxia impaired the heat tolerance of amphipods, especially starved ones. Fed amphipods likely rely more on anaerobic metabolism to maintain energy status during heat stress, whereas for starved amphipods aerobic metabolism appears to be more important. The depletion of their energy reserves constrains their ability to maintain energy status via anaerobic metabolism. We did not find evidence that alterations in heat tolerance following starvation were related to the upregulation of heat shock proteins. In conclusion, starvation can have opposite effects on heat tolerance, acting via pathways that are operating on different time scales.
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http://dx.doi.org/10.1016/j.cbpa.2020.110697DOI Listing
July 2020

Triploidy in zebrafish larvae: Effects on gene expression, cell size and cell number, growth, development and swimming performance.

PLoS One 2020 2;15(3):e0229468. Epub 2020 Mar 2.

Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, Nijmegen, The Netherlands.

There is renewed interest in the regulation and consequences of cell size adaptations in studies on understanding the ecophysiology of ectotherms. Here we test if induction of triploidy, which increases cell size in zebrafish (Danio rerio), makes for a good model system to study consequences of cell size. Ideally, diploid and triploid zebrafish should differ in cell size, but should otherwise be comparable in order to be suitable as a model. We induced triploidy by cold shock and compared diploid and triploid zebrafish larvae under standard rearing conditions for differences in genome size, cell size and cell number, development, growth and swimming performance and expression of housekeeping genes and hsp70.1. Triploid zebrafish have larger but fewer cells, and the increase in cell size matched the increase in genome size (+ 50%). Under standard conditions, patterns in gene expression, ontogenetic development and larval growth were near identical between triploids and diploids. However, under demanding conditions (i.e. the maximum swimming velocity during an escape response), triploid larvae performed poorer than their diploid counterparts, especially after repeated stimuli to induce swimming. This result is consistent with the idea that larger cells have less capacity to generate energy, which becomes manifest during repeated physical exertion resulting in increased fatigue. Triploidy induction in zebrafish appears a valid method to increase specifically cell size and this provides a model system to test for consequences of cell size adaptation for the energy budget and swimming performance of this ectothermic vertebrate.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0229468PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7051096PMC
June 2020

Effects of developmental plasticity on heat tolerance may be mediated by changes in cell size in Drosophila melanogaster.

Insect Sci 2020 Dec 17;27(6):1244-1256. Epub 2020 Jan 17.

Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, Nijmegen, The Netherlands.

There is a growing interest in the physiology underpinning heat tolerance of ectotherms and their responses to the ongoing rise in temperature. However, there is no consensus about the underlying physiological mechanisms. According to "the maintain aerobic scope and regulate oxygen supply" hypothesis, responses to warming at different organizational levels contribute to the ability to safeguard energy metabolism via aerobic pathways. At the cellular level, a decrease in cell size increases the capacity for the uptake of resources (e.g., food and oxygen), but the maintenance of electrochemical gradients across cellular membranes implies greater energetic costs in small cells. In this study, we investigated how different rearing temperatures affected cell size and heat tolerance in the fruit fly Drosophila melanogaster. We tested the hypothesis that smaller-celled flies are more tolerant to acute, intense heat stress whereas larger-celled flies are more tolerant to chronic, mild heat stress. We used the thermal tolerance landscape framework, which incorporates the intensity and duration of thermal challenge. Rearing temperatures strongly affected both cell size and survival times. We found different effects of developmental plasticity on tolerance to either chronic or acute heat stress. Warm-reared flies had both smaller cells and exhibited higher survival times under acute, intense heat stress when compared to cold-reared flies. However, under chronic, mild heat stress, the situation was reversed and cold-reared flies, consisting of larger cells, showed better survival. These differences in heat tolerance could have resulted from direct effects of rearing temperature or they may be mediated by the correlated changes in cell size. Notably, our results are consistent with the idea that a smaller cell size may confer tolerance to acute temperatures via enhanced oxygen supply, while a larger cell may confer greater tolerance to chronic and less intense heat stress via more efficient use of resources.
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http://dx.doi.org/10.1111/1744-7917.12742DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7687148PMC
December 2020

Thermal tolerance patterns across latitude and elevation.

Philos Trans R Soc Lond B Biol Sci 2019 08 17;374(1778):20190036. Epub 2019 Jun 17.

8 GloCEE - Global Change Ecology and Evolution Group, Department of Life Sciences, Universidad de Alcalá, 28805, Spain.

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'.
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http://dx.doi.org/10.1098/rstb.2019.0036DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6606462PMC
August 2019

Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers.

Philos Trans R Soc Lond B Biol Sci 2019 08 17;374(1778):20190035. Epub 2019 Jun 17.

1 Department of Animal Ecology and Physiology, Radboud University Nijmegen , 6500 Nijmegen , The Netherlands.

Global warming appears to favour smaller-bodied organisms, but whether larger species are also more vulnerable to thermal extremes, as suggested for past mass-extinction events, is still an open question. Here, we tested whether interspecific differences in thermal tolerance (heat and cold) of ectotherm organisms are linked to differences in their body mass and genome size (as a proxy for cell size). Since the vulnerability of larger, aquatic taxa to warming has been attributed to the oxygen limitation hypothesis, we also assessed how body mass and genome size modulate thermal tolerance in species with contrasting breathing modes, habitats and life stages. A database with the upper (CTmax) and lower (CTmin) critical thermal limits and their methodological aspects was assembled comprising more than 500 species of ectotherms. Our results demonstrate that thermal tolerance in ectotherms is dependent on body mass and genome size and these relationships became especially evident in prolonged experimental trials where energy efficiency gains importance. During long-term trials, CTmax was impaired in larger-bodied water-breathers, consistent with a role for oxygen limitation. Variation in CTmin was mostly explained by the combined effects of body mass and genome size and it was enhanced in larger-celled, air-breathing species during long-term trials, consistent with a role for depolarization of cell membranes. Our results also highlight the importance of accounting for phylogeny and exposure duration. Especially when considering long-term trials, the observed effects on thermal limits are more in line with the warming-induced reduction in body mass observed during long-term rearing experiments. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.
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http://dx.doi.org/10.1098/rstb.2019.0035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6606457PMC
August 2019

Human Monocyte-Derived Dendritic Cells Produce Millimolar Concentrations of ROS in Phagosomes Per Second.

Front Immunol 2019 29;10:1216. Epub 2019 May 29.

Tumor Immunology Lab, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Nijmegen, Netherlands.

Neutrophils kill ingested pathogens by the so-called oxidative burst, where reactive oxygen species (ROS) are produced in the lumen of phagosomes at very high rates (mM/s), although these rates can only be maintained for a short period (minutes). In contrast, dendritic cells produce ROS at much lower rates, but they can sustain production for much longer after pathogen uptake (hours). It is becoming increasingly clear that this slow but prolonged ROS production is essential for antigen cross-presentation to activate cytolytic T cells, and for shaping the repertoire of antigen fragments for presentation to helper T cells. However, despite this importance of ROS production by dendritic cells for activation of the adaptive immune system, their actual ROS production rates have never been quantified. Here, we quantified ROS production in human monocyte-derived dendritic cells by measuring the oxygen consumption rate during phagocytosis. Although a large variation in oxygen consumption and phagocytic capacity was present among individuals and cells, we estimate a ROS production rate of on average ~0.5 mM/s per phagosome. Quantitative microscopy approaches showed that ROS is produced within minutes after pathogen encounter at the nascent phagocytic cup. HDCFDA measurements revealed that ROS production is sustained for at least ~10 h after uptake. While ROS are produced by dendritic cells at an about 10-fold lower rate than by neutrophils, the net total ROS production is approximately similar. These are the first quantitative estimates of ROS production by a cell capable of antigen cross-presentation. Our findings provide a quantitative insight in how ROS affect dendritic cell function.
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http://dx.doi.org/10.3389/fimmu.2019.01216DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6548834PMC
July 2020

Differences in the respiratory response to temperature and hypoxia across four life-stages of the intertidal porcelain crab .

Mar Biol 2018 23;165(9):146. Epub 2018 Aug 23.

1Centro i~mar, Universidad de Los Lagos, Casilla 557, Puerto Montt, Chile.

For aquatic breathers, hypoxia and warming can act synergistically causing a mismatch between oxygen supply (reduced by hypoxia) and oxygen demand (increased by warming). The vulnerability of these species to such interactive effects may differ during ontogeny due to differing gas exchange systems. This study examines respiratory responses to temperature and hypoxia across four life-stages of the intertidal porcelain crab . Eggs, megalopae, juveniles and adults were exposed to combinations of temperatures from 6 to 18 °C and oxygen tensions from 2 to 21 kPa. Metabolic rates differed strongly across life-stages which could be partly attributed to differences in body mass. However, eggs exhibited significantly lower metabolic rates than predicted for their body mass. For the other three stages, metabolic rates scaled with a mass exponent of 0.89. Mass scaling exponents were similar across all temperatures, but were significantly influenced by oxygen tension (the highest at 9 and 14 kPa, and the lowest at 2 kPa). Respiratory responses across gradients of oxygen tension were used to calculate the response to hypoxia, whereby eggs, megalopae and juveniles responded as oxyconformers and adults as oxyregulators. The thermal sensitivity of the metabolic rates () were dependent on the oxygen tension in megalopae, and also on the interaction between oxygen tension and temperature intervals in adults. Our results thus provide evidence on how the oxygen tension can modulate the mass dependence of metabolic rates and demonstrate changes in respiratory control from eggs to adults. In light of our results indicating that adults show a good capacity for maintaining metabolism independent of oxygen tension, our study highlights the importance of assessing responses to multiple stressors across different life-stages to determine how vulnerability to warming and hypoxia changes during development.
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http://dx.doi.org/10.1007/s00227-018-3406-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6132507PMC
August 2018

Foundation species enhance food web complexity through non-trophic facilitation.

PLoS One 2018 31;13(8):e0199152. Epub 2018 Aug 31.

Institute of Water and Wetland Research, Radboud University Nijmegen, Nijmegen, the Netherlands.

Food webs are an integral part of every ecosystem on the planet, yet understanding the mechanisms shaping these complex networks remains a major challenge. Recently, several studies suggested that non-trophic species interactions such as habitat modification and mutualisms can be important determinants of food web structure. However, it remains unclear whether these findings generalize across ecosystems, and whether non-trophic interactions affect food webs randomly, or affect specific trophic levels or functional groups. Here, we combine analyses of 58 food webs from seven terrestrial, freshwater and coastal systems to test (1) the general hypothesis that non-trophic facilitation by habitat-forming foundation species enhances food web complexity, and (2) whether these enhancements have either random or targeted effects on particular trophic levels, functional groups, and linkages throughout the food web. Our empirical results demonstrate that foundation species consistently enhance food web complexity in all seven ecosystems. Further analyses reveal that 15 out of 19 food web properties can be well-approximated by assuming that foundation species randomly facilitate species throughout the trophic network. However, basal species are less strongly, and carnivores are more strongly facilitated in foundation species' food webs than predicted based on random facilitation, resulting in a higher mean trophic level and a longer average chain length. Overall, we conclude that foundation species strongly enhance food web complexity through non-trophic facilitation of species across the entire trophic network. We therefore suggest that the structure and stability of food webs often depends critically on non-trophic facilitation by foundation species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0199152PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6118353PMC
January 2019

It's about time: Linkages between heat tolerance, thermal acclimation and metabolic rate at different temporal scales in the freshwater amphipod Gammarus fossarum Koch, 1836.

J Therm Biol 2018 Jul 1;75:31-37. Epub 2018 May 1.

Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010, GL, Heyendaelseweg 135, 6525 AJ Nijmegen, The Netherlands. Electronic address:

Temperature has a profound impact on ectotherms. Warming increases the metabolic oxygen demand of ectotherms, which could result in a mismatch between their oxygen demand and their ability to extract and deliver sufficient oxygen to meet demand. This hypothesis has been mainly tested using short-term exposure to intense thermal stress. However, the thermal responses of organisms can be different on longer timescales, where physiological acclimation becomes increasingly important. Such thermal acclimation effects may reduce the vulnerability of ectotherms to warming on the long term. Thus, responses to intense, short-term thermal stress may be different from responses to moderate, prolonged thermal stress. Here, we examine the effect of thermal acclimation on heat tolerance and metabolism in the aquatic ectotherm Gammarus fossarum (Koch, 1836). Amphipods were acclimated to either 11.1 ± 0.1 °C or 19.8 ± 0.1 °C and after thermal acclimation we measured both their metabolism and their survival time at different temperatures. Our results show that metabolism strongly increased with increasing temperatures in the cold-acclimated group, but less so in the warm-acclimated group. Cold-acclimated amphipods were also more sensitive to thermal stress, especially during prolonged exposure. Thus, the differences between both thermal acclimation groups support the idea of oxygen-limited heat tolerance: cold-acclimated amphipods showed increased oxygen consumption and decreased thermal tolerance. However, across individuals, those that sharply increased oxygen consumption with increasing temperature did not differ in heat tolerance from individuals whose metabolism was much less sensitive to temperature. Thus, acclimation to different temperatures appeared to be beneficial, but a role for oxygen limitation could not be demonstrated unambiguously. Beneficial effect of acclimation were much larger during prolonged exposure, with the acclimation response ratio (ARR) ranging from 0.03 to over 0.5 depending on the time scale (minutes to months). Thus, the acclimatory capacity may have been underestimated by short-term experimental studies.
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http://dx.doi.org/10.1016/j.jtherbio.2018.04.016DOI Listing
July 2018

Thermal limits in native and alien freshwater peracarid Crustacea: The role of habitat use and oxygen limitation.

Funct Ecol 2018 Apr 6;32(4):926-936. Epub 2018 Feb 6.

Institute of Landscape Ecology University of Münster Münster Germany.

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). 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, and , showed little response to oxygen conditions in their CTmax, whereas the CTmax of heat-sensitive species, for example, s and , 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 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 is the more likely dominant alien species. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13050/suppinfo is available for this article.
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http://dx.doi.org/10.1111/1365-2435.13050DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5993316PMC
April 2018

The limits of respiratory function: External and internal constraints on insect gas exchange.

J Insect Physiol 2018 04;106(Pt 3):153-154

Department of Animal Ecology and Ecophysiology, Radboud University, Nijmegen.

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http://dx.doi.org/10.1016/j.jinsphys.2018.04.011DOI Listing
April 2018

The temperature-size rule in across different genetic lines and ontogenetic stages: Multiple patterns and mechanisms.

Ecol Evol 2018 Apr 13;8(8):3828-3841. Epub 2018 Mar 13.

Department of Animal Ecology and Physiology Radboud University Nijmegen The Netherlands.

Ectotherms tend to grow faster, but reach a smaller size when reared under warmer conditions. This temperature-size rule (TSR) is a widespread phenomenon. Despite the generality of this pattern, no general explanation has been found. We therefore tested the relative importance of two proposed mechanisms for the TSR: (1) a stronger increase in development rate relative to growth rate at higher temperatures, which would cause a smaller size at maturity, and (2) resource limitation placing stronger constraints on growth in large individuals at higher temperatures, which would cause problems with attaining a large size in warm conditions. We raised at eight temperatures to assess their size at maturity, asymptotic size, and size of their offspring. We used three clonal lines that differed in asymptotic size and growth rate. A resource allocation model was developed and fitted to our empirical data to explore the effect of both mechanisms for the TSR. The genetic lines of showed different temperature dependence of growth and development rates resulting in different responses for size at maturity. Also, at warm temperatures, growth was constrained in large, but not in small individuals. The resource allocation model could fit these empirical data well. Based on our empirical results and model explorations, the TSR of at maturity is best explained by a stronger increase in development rate relative to growth rate at high temperature, and the TSR at asymptotic size is best explained by a size-dependent and temperature-dependent constraint on growth, although resource limitation could also affect size at maturity. In conclusion, the TSR can take different forms for offspring size, size at maturity, and asymptotic size and each form can arise from its own mechanism, which could be an essential step toward finding a solution to this century-old puzzle.
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http://dx.doi.org/10.1002/ece3.3933DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5916275PMC
April 2018

Functional Hypoxia in Insects: Definition, Assessment, and Consequences for Physiology, Ecology, and Evolution.

Annu Rev Entomol 2018 01 6;63:303-325. Epub 2017 Oct 6.

Department of Animal Ecology and Ecophysiology, Radboud University, Nijmegen, Netherlands; email:

Insects can experience functional hypoxia, a situation in which O 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 availability or transport capacities and when O need is great. Functional hypoxia occurs normally during insect development and is a factor in mediating life-history trade-offs.
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http://dx.doi.org/10.1146/annurev-ento-020117-043145DOI Listing
January 2018

Long-term and acute effects of temperature and oxygen on metabolism, food intake, growth and heat tolerance in a freshwater gastropod.

J Therm Biol 2017 Aug 1;68(Pt A):27-38. Epub 2016 Dec 1.

Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University, P.O. Box 9010, 6500 GL, Nijmegen, The Netherlands. Electronic address:

Temperature affects the physiology and life-history of ectothermic animals, often increasing metabolic rate and decreasing body size. Oxygen limitation has been put forward as a mechanism to explain thermal responses of body size and the ability to survive stress. However the time-scales involved in growth performance and heat tolerance differ radically. In order to increase our understanding of oxygen and temperature effects on body size and heat tolerance and the time scale involved, we reared Lymnaea stagnalis under six combinations of temperature and oxygen tension from hatching up to an age of 300 days and recorded shell length during this whole period. At the end of this period, we determined scope for growth by measuring food intake rate, assimilation efficiency, respiration rate and ammonium excretion rate at two different temperatures. We also measured the snails' ability to survive heat stress (CTmax), both at normoxia and hypoxia. We found that scope for growth and long term growth performance were much more affected by interactions of chronic oxygen and temperature conditions during rearing than by acute conditions during testing. Furthermore, our study shows that individual variation in growth performance can be traced back to individual differences in rates of food and oxygen consumption. Developmental acclimation also gave rise to differences in CTmax, but these were relatively small and were only expressed when CTmax was tested under hypoxia. The large effects of rearing oxygen conditions on growth and other physiological rates compared to modest effects of test oxygen conditions on CTmax suggest that small effects of hypoxia on the short term (e.g. heat tolerance) may nevertheless have large repercussions on the long term (e.g. growth and reproduction), even in a pulmonate snail that can compensate for hypoxia to some extent by aerial respiration.
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http://dx.doi.org/10.1016/j.jtherbio.2016.11.017DOI Listing
August 2017

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

Glob Chang Biol 2016 May 29;22(5):1769-78. Epub 2016 Feb 29.

Catchment Research Group, Cardiff School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK.

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.
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http://dx.doi.org/10.1111/gcb.13240DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5324560PMC
May 2016

Is the temperature-size rule mediated by oxygen in aquatic ectotherms?

J Therm Biol 2015 Dec 9;54:56-65. Epub 2014 Dec 9.

Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010,6500 GL, Heyendaelseweg 135, 6525 AJ Nijmegen, The Netherlands. Electronic address:

Temperature is an important environmental factor that influences key traits like body size, growth rate and maturity. Ectotherms reared under high temperatures usually show faster growth, but reach a smaller final size, a phenomenon known as the temperature-size rule (TSR). Oxygen may become a limiting resource at high temperatures, when demand for oxygen is high, especially in water as oxygen uptake is far more challenging under water than in air. Therefore, in aquatic ectotherms, the TSR might very well be mediated by temperature effects on oxygen availability and oxygen demand. To distinguish between the direct effects of temperature and oxygen mediated effects, growth rate and final size were measured in the aquatic ectotherm Asellus aquaticus (Linnaeus, 1758) reared under different temperature and oxygen conditions in a factorial design. Growth could be best described by a modified Von Bertalanffy growth function. Both temperature and oxygen affected age at maturity and growth. Growth responses to temperature were dependent on oxygen conditions (interactive effect of temperature and oxygen). Only under hypoxic conditions, when oxygen was most limiting, did we find a classic TSR. Moreover, when comparing treatments differing in temperature, but where the balance between oxygen demand and supply was similar, high temperature increased both growth rate and final size. Thus effects of oxygen may resolve the life-history puzzle of the TSR in aquatic ectotherms.
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http://dx.doi.org/10.1016/j.jtherbio.2014.12.003DOI Listing
December 2015

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

Comp Biochem Physiol A Mol Integr Physiol 2016 Feb 24;192:64-78. Epub 2015 Oct 24.

Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Stellenbosch University, South Africa.

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.
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http://dx.doi.org/10.1016/j.cbpa.2015.10.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4717866PMC
February 2016

Can respiratory physiology predict thermal niches?

Ann N Y Acad Sci 2016 Feb 31;1365(1):73-88. Epub 2015 Aug 31.

Department of Integrative Ecophysiology, Alfred-Wegener-Institute for Polar and Marine Research, Bremerhaven, Germany.

Predicting species responses to global warming is the holy grail of climate change science. As temperature directly affects physiological rates, it is clear that a mechanistic understanding of species vulnerability should be grounded in organismal physiology. Here, we review what respiratory physiology can offer the field of thermal ecology, showcasing different perspectives on how respiratory physiology can help explain thermal niches. In water, maintaining adequate oxygen delivery to fuel the higher metabolic rates under warming conditions can become the weakest link, setting thermal tolerance limits. This has repercussions for growth and scaling of metabolic rate. On land, water loss is more likely to become problematic as long as O2 delivery and pH balance can be maintained, potentially constraining species in their normal activity. Therefore, high temperatures need not be lethal, but can still affect the energy intake of an animal, with concomitant consequences for long-term fitness. While respiratory challenges and adaptive responses are diverse, there are clear recurring elements such as oxygen uptake, CO2 excretion, and water homeostasis. We show that respiratory physiology has much to offer the field of thermal ecology and call for an integrative, multivariate view incorporating respiratory challenges, thermal responses, and energetic consequences. Fruitful areas for future research are highlighted.
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http://dx.doi.org/10.1111/nyas.12876DOI Listing
February 2016

Species-area relationships are modulated by trophic rank, habitat affinity, and dispersal ability.

Ecology 2015 Feb;96(2):518-31

In the face of ongoing habitat fragmentation, species-area relationships (SARs) have gained renewed interest and are increasingly used to set conservation priorities. An important question is how large habitat areas need to be to optimize biodiversity conservation. The relationship between area and species richness is explained by colonization-extinction dynamics, whereby smaller sites harbor smaller populations, which are more prone to extinction than the larger populations sustained by larger sites. These colonization-extinction dynamics are predicted to vary with trophic rank, habitat affinity, and dispersal ability of the species. However, empirical evidence for the effect of these species characteristics on SARs remains inconclusive. In this study we used carabid beetle data from 58 calcareous grassland sites to investigate how calcareous grassland area affects species richness and activity density for species differing in trophic rank, habitat affinity, and dispersal ability. In addition, we investigated how SARs are affected by the availability of additional calcareous grassland in the surrounding landscape. Beetle species richness and activity density increased with calcareous grassland area for zoophagous species that are specialists for dry grasslands and, to a lesser extent, for zoophagous habitat generalists. Phytophagous species and zoophagous forest and wet-grassland specialists were not affected by calcareous grassland area. The dependence of species on large single sites increased with decreasing dispersal ability for species already vulnerable to calcareous grassland area. Additional calcareous grassland in the landscape had a positive effect on local species richness of both dry-grassland specialists and generalists, but this effect was restricted to a few hundred meters. Our results demonstrate that SARs are affected by trophic rank, habitat affinity, and dispersal ability. These species characteristics do not operate independently, but should be viewed in concert. In addition, species' responses depend on the landscape context. Our study suggests that the impact of habitat area on trophic interactions may be larger than previously anticipated. In small habitat fragments surrounded by a hostile matrix, food chains may be strongly disrupted. This highlights the need to conserve continuous calcareous grassland patches of at least several hectares in size.
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http://dx.doi.org/10.1890/14-0082.1DOI Listing
February 2015

Oxygen-limited thermal tolerance is seen in a plastron-breathing insect and can be induced in a bimodal gas exchanger.

J Exp Biol 2015 Jul 11;218(Pt 13):2083-8. Epub 2015 May 11.

Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, University of Plymouth, Davy Building, Drake Circus, Plymouth PL4 8AA, UK.

Thermal tolerance has been hypothesized to result from a mismatch between oxygen supply and demand. However, the generality of this hypothesis has been challenged by studies on various animal groups, including air-breathing adult insects. Recently, comparisons across taxa have suggested that differences in gas exchange mechanisms could reconcile the discrepancies found in previous studies. Here, we test this suggestion by comparing the behaviour of related insect taxa with different gas exchange mechanisms, with and without access to air. We demonstrate oxygen-limited thermal tolerance in air-breathing adults of the plastron-exchanging water bug Aphelocheirus aestivalis. Ilyocoris cimicoides, a related, bimodal gas exchanger, did not exhibit such oxygen-limited thermal tolerance and relied increasingly on aerial gas exchange with warming. Intriguingly, however, when denied access to air, oxygen-limited thermal tolerance could also be induced in this species. Patterns in oxygen-limited thermal tolerance were found to be consistent across life-history stages in these insects, with nymphs employing the same gas exchange mechanisms as adults. These results advance our understanding of oxygen limitation at high temperatures; differences in the degree of respiratory control appear to modulate the importance of oxygen in setting tolerance limits.
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http://dx.doi.org/10.1242/jeb.119560DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4510840PMC
July 2015

Native and non-native plants provide similar refuge to invertebrate prey, but less than artificial plants.

PLoS One 2015 17;10(4):e0124455. Epub 2015 Apr 17.

Department of Aquatic Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, the Netherlands.

Non-native species introductions are widespread and can affect ecosystem functioning by altering the structure of food webs. Invading plants often modify habitat structure, which may affect the suitability of vegetation as refuge and could thus impact predator-prey dynamics. Yet little is known about how the replacement of native by non-native vegetation affects predator-prey dynamics. We hypothesize that plant refuge provisioning depends on (1) the plant's native status, (2) plant structural complexity and morphology, (3) predator identity, and (4) prey identity, as well as that (5) structurally similar living and artificial plants provide similar refuge. We used aquatic communities as a model system and compared the refuge provided by plants to macroinvertebrates (Daphnia pulex, Gammarus pulex and damselfly larvae) in three short-term laboratory predation experiments. Plant refuge provisioning differed between plant species, but was generally similar for native (Myriophyllum spicatum, Ceratophyllum demersum, Potamogeton perfoliatus) and non-native plants (Vallisneria spiralis, Myriophyllum heterophyllum, Cabomba caroliniana). However, plant refuge provisioning to macroinvertebrate prey depended primarily on predator (mirror carp: Cyprinus carpio carpio and dragonfly larvae: Anax imperator) and prey identity, while the effects of plant structural complexity were only minor. Contrary to living plants, artificial plant analogues did improve prey survival, particularly with increasing structural complexity and shoot density. As such, plant rigidity, which was high for artificial plants and one of the living plant species evaluated in this study (Ceratophyllum demersum), may interact with structural complexity to play a key role in refuge provisioning to specific prey (Gammarus pulex). Our results demonstrate that replacement of native by structurally similar non-native vegetation is unlikely to greatly affect predator-prey dynamics. We propose that modification of predator-prey interactions through plant invasions only occurs when invading plants radically differ in growth form, density and rigidity compared to native plants.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0124455PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4401678PMC
April 2016

Respiratory control in aquatic insects dictates their vulnerability to global warming.

Biol Lett 2013 Oct 7;9(5):20130473. Epub 2013 Aug 7.

Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University, Nijmegen, The Netherlands.

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.
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http://dx.doi.org/10.1098/rsbl.2013.0473DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971685PMC
October 2013

Niche segregation in two closely related species of stickleback along a physiological axis: explaining multidecadal changes in fish distribution from iron-induced respiratory impairment.

Aquat Ecol 2012;46(2):241-248. Epub 2012 Apr 21.

Experimental Zoology Group, Department of Animal Sciences, Wageningen University, De Elst 1, 6708 WD Wageningen, The Netherlands.

Acute exposure to iron can be lethal to fish, but long-term sublethal impacts of iron require further study. Here we investigated whether the spatial and temporal distribution (1967-2004) of two closely related species of stickleback matched the spatial distribution of iron concentrations in the groundwater. We used the 'Northern Peel region', a historically iron-rich peat landscape in The Netherlands as a case study. This allowed us to test the hypothesis that niche segregation in two closely related species of stickleback occurred along a physiological axis. Patterns in stickleback occurrence were strongly associated with spatial patterns in iron concentrations before 1979: iron-rich grid cells were avoided by three-spined stickleback (, Linnaeus 1758) and preferred by nine-spined stickleback (, [Linnaeus, 1758]). After 1979, the separation between both sticklebacks became weaker, corresponding to a decreased influence of local groundwater on stream water quality. The way both species changed their distribution in the field provides a strong indication that they differ in their susceptibility to iron-rich conditions. These observed differences correspond with differences in their respiration physiology, tolerance of poor oxygen conditions and overall life-history strategy documented in the literature. Our results exemplify how species can partition niche along a non-structural niche axis, such as sublethal iron-rich conditions. Other fish species may similarly segregate along concentration gradients in iron, while sublethal concentrations of other metals such as copper may similarly impact fish via respiratory impairment and reduced aerobic scope.
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http://dx.doi.org/10.1007/s10452-012-9395-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4431660PMC
April 2012

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

Ecology 2011 Aug;92(8):1565-72

Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, University of Plymouth, Davy Building, Drake Circus, Plymouth PL48AA, United Kingdom.

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 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.
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http://dx.doi.org/10.1890/10-2369.1DOI Listing
August 2011