Temperature, productivity, and habitat characteristics collectively drive lake food web structure.

While many efforts have been devoted to understand variations in food web structure among terrestrial and aquatic ecosystems, the environmental factors influencing food web structure at large spatial scales remain hardly explored. Here, we compiled biodiversity inventories to infer food web structure of 67 French lakes using an allometric niche-based model and tested how environmental variables (temperature, productivity, and habitat) influence them. By applying a multivariate analysis on 20 metrics of food web topology, we found that food web structural variations are represented by two distinct complementary and independent structural descriptors. The first is related to the overall trophic diversity, whereas the second is related to the vertical structure. Interestingly, the trophic diversity descriptor was mostly explained by habitat size (26.7% of total deviance explained) and habitat complexity (20.1%) followed by productivity (dissolved organic carbon: 16.4%; nitrate: 9.1%) and thermal variations (10.7%). Regarding the vertical structure descriptor, it was mostly explained by water thermal seasonality (39.0% of total deviance explained) and habitat depth (31.9%) followed by habitat complexity (8.5%) and size (5.5%) as well as annual mean temperature (5.6%). Overall, we found that temperature, productivity, and habitat characteristics collectively shape lake food web structure. We also found that intermediate levels of productivity, high levels of temperature (mean and seasonality), as well as large habitats are associated with the largest and most complex food webs. Our findings, therefore, highlight the importance of focusing on these three components especially in the context of global change, as significant structural changes in aquatic food webs could be expected under increased temperature, pollution, and habitat alterations.

Variation of thermal plasticity in growth and reproduction patterns: Importance of ancestral and developmental temperatures.

Temperature is an important ecological driver modulating life history traits of organisms, such as growth and reproduction. With the ongoing global warming, understanding the mechanisms underlying the effect of temperature on size and resource allocation trade-off is crucial. The temperature-size rule (TSR) describes plastic growth patterns in populations of ectothermic species under different thermal environments, whereby warming results in faster initial growth but lower size at maturity. However, the evolution of the TSR remains poorly understood. Here we conducted an experiment with populations of the medaka fish Oryzias latipes maintained at two temperatures for successive generations to investigate changes in the growth pattern of the TSR. After rearing six generations at cold (20 °C) and warm (30 °C) temperature, we conducted common garden experiments on the seventh generation where we compare growth trajectories and reproduction patterns in four different groups of fish: (i) fish reared at cold temperature over all seven generations (cold past and present), (ii) fish reared at warm temperature over six generations and at cold temperature at the seventh generation (warm past and cold present), (iii) fish reared at warm temperature over all seven generations (warm past and present) and (iv) fish reared at cold temperature over six generations and at warm temperature at the seventh generation (cold past and warm present). For each treatment, we monitored growth curves and reproduction, and investigated changes in model parameters and reproduction up to 350 days after hatching. Our study showed changes in TSR patterns according to ancestral and developmental temperatures. Developmental temperature mainly impacted age at maturity and asymptotic size, whereas size at maturity was driven more by the dissimilarity between developmental and ancestral temperatures. Our results also highlight a loss of plasticity in temperature-size and reproductive patterns for the fish that were reared under warm condition over six generations.

Multigenerational exposure to temperature influences mitochondrial oxygen fluxes in the Medaka fish (Oryzias latipes).

AIM: Thermal sensitivity of cellular metabolism is crucial for animal physiology and survival under climate change. Despite recent efforts, effects of multigenerational exposure to temperature on the metabolic functioning remain poorly understood. We aimed at determining whether multigenerational exposure to temperature modulate the mitochondrial respiratory response of Medaka fish. METHODS: We conducted a multigenerational exposure with Medaka fish reared multiple generations at 20 and 30°C (COLD and WARM fish, respectively). We then measured the oxygen consumption of tail muscle at two assay temperatures (20 and 30°C). Mitochondrial function was determined as the respiration supporting ATP synthesis (OXPHOS) and the respiration required to offset proton leak (LEAK(Omy)) in a full factorial design (COLD-20°C; COLD-30°C; WARM-20°C; WARM-30°C). RESULTS: We found that higher OXPHOS and LEAK fluxes at 30°C compared to 20°C assay temperature. At each assay temperature, WARM fish had lower tissue oxygen fluxes than COLD fish. Interestingly, we did not find significant differences in respiratory flux when mitochondria were assessed at the rearing temperature of the fish (i.e., COLD-20°C vs. WARM -30°C). CONCLUSION: The lower OXPHOS and LEAK capacities in warm fish are likely the result of the multigenerational exposure to warm temperature. This is consistent with a modulatory response of mitochondrial capacity to compensate for potential detrimental effects of warming on metabolism. Finally, the absence of significant differences in respiratory fluxes between COLD-20°C and WARM-30°C fish likely reflects an optimal respiration flux when organisms adapt to their thermal conditions.

Distinct impacts of feeding frequency and warming on life history traits affect population fitness in vertebrate ectotherms.

Body size shifts in ectotherms are mostly attributed to the Temperature Size Rule (TSR) stating that warming speeds up initial growth rate but leads to smaller size when food does not limit growth. Investigating the links between temperature, growth, and life history traits is key to understand the adaptive value of TSR, which might be context dependent. In particular, global warming can affect food quantity or quality which is another major driver of growth, fecundity, and survival. However, we have limited information on how temperature and food jointly influence life history traits in vertebrate predators and how changes in different life history traits combine to influence fitness and population demography. We investigate (1) whether TSR is maintained under different food conditions, (2) if food exacerbates or dampens the effects of temperature on growth and life history traits and (3) if food influences the adaptive value of TSR. We combine experiments on the medaka with Integral Projection Models to scale from life history traits to fitness consequences. Our results confirm that warming triggers a higher initial growth rate and a lower adult size, reduces generation time and increases mean fitness. A lower level of food exacerbates the effects of warming on growth trajectories. Although lower feeding frequency increased survival and decreased fecundity, it did not influence the effects of warming on fish development rates, fecundity, and survival. In contrast, feeding frequency influenced the adaptive value of TSR, as, under intermittent feeding, generation time decreased faster with warming and the increase in growth rate with warming was weaker compared to continuously fed fish. These results are of importance in the context of global warming as resources are expected to change with increasing temperatures but, surprisingly, our results suggest that feeding frequency have a lower impact on fitness at high temperature.

Evolution of pace-of-life syndrome under conditions of maternal PCB contamination and global warming in early life stages of cold stenothermic fish (Arctic char).

The end of the 20th century was characterised by rapid modifications of ecosystem functioning under different pressures (such as eutrophication and toxic pollution). Increasing temperatures in the context of global warming could have indirect consequences, such as increased bioavailability of hydrophobic organic pollutants amongst aquatic species. According to the "pace-of-life syndrome" (POLS) theory, these stressors could lead to covariations in many life traits. Lake Bourget is the largest natural lake in France and has been highly polluted from the fifties to the eighties both with a high load of nutrients (wastewater discharge) and polychlorinated biphenyls (PCBs) (industrial effluent discharge). Despite improvements in water quality since the 21st century, PCB levels are still higher than the United States Environmental Protection Agency cut-off for wildlife protection. The population of Arctic char, a cold stenothermic salmonid, has remained low in Lake Bourget for the last ten years despite restocking efforts and complete re-oligotrophication. We hypothesised that PCB pollution can affect the Arctic char population and that the increase in water temperature could magnify the effects of PCB. Thus, this study aimed to investigate the effects of maternal PCB contamination on offspring using a multiparametric and multiscale approach. Female Arctic char were contaminated with PCB before spawning, and each fertilised spawn was incubated at two temperatures (4 and 8.5 °C). The results showed that co-exposure to increased temperature and maternal PCB contamination influenced biodemographic, physiological, and behavioural parameters. The effects were highly dependant on the developmental stage. Based on the POLS theory, a continuum of life traits that may reflect potential physiological and behavioural modifications in response to these concurrent stressors is highlighted.

Global warming benefits the small in aquatic ecosystems.

Understanding the ecological impacts of climate change is a crucial challenge of the twenty-first century. There is a clear lack of general rules regarding the impacts of global warming on biota. Here, we present a metaanalysis of the effect of climate change on body size of ectothermic aquatic organisms (bacteria, phyto- and zooplankton, and fish) from the community to the individual level. Using long-term surveys, experimental data and published results, we show a significant increase in the proportion of small-sized species and young age classes and a decrease in size-at-age. These results are in accordance with the ecological rules dealing with the temperature-size relationships (i.e., Bergmann's rule, James' rule and Temperature-Size Rule). Our study provides evidence that reduced body size is the third universal ecological response to global warming in aquatic systems besides the shift of species ranges toward higher altitudes and latitudes and the seasonal shifts in life cycle events.

Ecosystem maturity modulates greenhouse gases fluxes from artificial lakes.

Lentic ecosystems play a major role in the global carbon cycling but the understanding of the environmental determinants of lake metabolism is still limited, notably in small artificial lakes. Here the effects of environmental conditions on lake metabolism and CO2 and CH4 emissions were quantified in 11 small artificial gravel pit lakes covering a gradient of ecosystem maturity, ranging from young oligotrophic to older, hypereutrophic lakes. The diffusive fluxes of CO2 and CH4 ranged from -30.10 to 37.78 mmol m-2 d-1 and from 3.05 to 25.45 mmol m-2 d-1 across gravel pit lakes, respectively. Nutrients and chlorophyll a concentrations were negatively correlated with CO2 concentrations and emissions but positively correlated with CH4 concentrations and emissions from lakes. These findings indicate that, as they mature, gravel pit lakes switch from heterotrophic to autotrophic-based metabolism and hence turn into CO2-sinks. In contrast, the emission of CH4 increased along the maturity gradient. As a result, eutrophication occurring during ecosystem maturity increased net emissions in terms of climate impact (CO2 equivalent) due to the higher contribution of CH4 emissions. Overall, mean CO2equivalent emission was 7.9 g m-2 d-1, a value 3.7 and 4.7 times higher than values previously reported in temperate lakes and reservoirs, respectively. While previous studies reported that lakes represent emitters of C to the atmosphere, this study highlights that eutrophication may reverse lake contribution to global C budgets. However, this finding is to be balanced with the fact that eutrophication also increased CH4 emissions and hence, enhanced the potential impact of these ecosystems on climate. Implementing mitigation strategies for maintaining intermediate levels of maturity is therefore needed to limit the impacts of small artificial waterbodies on climate. This could be facilitated by their small size and should be planned at the earliest stages of artificial lake construction.

Assessing the ecological status in the context of the European Water Framework Directive: where do we go now?

The Water Framework Directive (WFD) is now well established as the key management imperative in river basins across Europe. However, there remain significant concerns with the way WFD is implemented and there is now a need for water managers and scientists to communicate better in order to find solutions to these concerns. To address this, a Science-Policy Interface (SPI) activity was launched in 2010 led by Directorate-General for Research and Innovation and Onema (the French national agency for water and aquatic ecosystems), which provided an interactive forum to connect scientists and WFD end-users. One major aim of the SPI activity was to establish a list of the most crucial research and development needs for enhancing WFD implementation. This paper synthesises the recommendations from this event highlighting 10 priority issues relating to ecological status. For lakes, temporary streams and transitional and coastal waters, WFD implementation still suffers from a lack of WFD-compliant bioassessment methods. For rivers, special attention is required to assess the ecological impacts of hydromorphological alterations on biological communities, notably those affecting river continuity and riparian covering. Spatial extrapolation tools are needed in order to evaluate ecological status for water bodies for which no data are available. The need for more functional bioassessment tools as complements to usual WFD-compliant tools, and to connect clearly good ecological state, biodiversity and ecosystem services when implementing WFD were also identified as crucial issues.

Temperature-size relations from the cellular-genomic perspective.

A family of empirically based ecological 'rules', collectively known as temperature-size rules, predicts larger body size in colder environments. This prediction is based on studies demonstrating that a wide range of ectotherms show increased body size, cell size or genome size in low-temperature habitats, or that individuals raised at low temperature become larger than conspecifics raised at higher temperature. There is thus a potential for reduction in size with global warming, affecting all levels from cell volume to body size, community composition and food webs. Increased body size may be obtained either by increasing the size or number of cells. Processes leading to changed cell size are of great interest from an ecological, physiological and evolutionary perspective. Cell size scales with fundamental properties such as genome size, growth rate, protein synthesis rates and metabolic activity, although the causal directions of these correlations are not clear. Changes in genome size will thus, in many cases, not only affect cell or body size, but also life-cycle strategies. Symmetrically, evolutionary drivers of life-history strategies may impact growth rate and thus cell size, genome size and metabolic rates. Although this goes to the core of many ecological processes, it is hard to move from correlations to causations. To the extent that temperature-driven changes in genome size result in significant differences among populations in body size, allometry or life-cycle events such as mating season, it could serve as a fast route to speciation. We offer here a novel perspective on the temperature-size rules from a 'bottom-up' perspective: how temperature may induce changes in genome size, and thus implicitly in cell size and body size of metazoans. Alternatively: how temperature-driven enlargement of cells also dictates genome-size expansion to maintain the genome-size to cell-volume ratio. We then discuss the different evolutionary drivers in aquatic versus terrestrial systems, and whether it is possible to arrive at a unifying theory that also may serve as a predictive tool related to temperature changes. This, we believe, will offer an updated review of a basic concept in ecology, and novel perspectives on the basic biological responses to temperature changes from a genomic perspective.

A new freshwater biodiversity indicator based on fish community assemblages.

Biodiversity has reached a critical state. In this context, stakeholders need indicators that both provide a synthetic view of the state of biodiversity and can be used as communication tools. Using river fishes as model, we developed community indicators that aim at integrating various components of biodiversity including interactions between species and ultimately the processes influencing ecosystem functions. We developed indices at the species level based on (i) the concept of specialization directly linked to the niche theory and (ii) the concept of originality measuring the overall degree of differences between a species and all other species in the same clade. Five major types of originality indices, based on phylogeny, habitat-linked and diet-linked morphology, life history traits, and ecological niche were analyzed. In a second step, we tested the relationship between all biodiversity indices and land use as a proxy of human pressures. Fish communities showed no significant temporal trend for most of these indices, but both originality indices based on diet- and habitat- linked morphology showed a significant increase through time. From a spatial point of view, all indices clearly singled out Corsica Island as having higher average originality and specialization. Finally, we observed that the originality index based on niche traits might be used as an informative biodiversity indicator because we showed it is sensitive to different land use classes along a landscape artificialization gradient. Moreover, its response remained unchanged over two other land use classifications at the global scale and also at the regional scale.

Impacts of global changes and extreme hydroclimatic events on macroinvertebrate community structures in the French Rhône River.

We assessed the temporal changes in and the relationships between the structures of the macroinvertebrate communities and the environmental conditions of the French Rhône River (the river from Lake Geneva to the Mediterranean Sea) over the last 20 years (1985-2004). Multisite environmental and biological datasets were analysed using multiple CO-inertia analysis (MCOA) and Procrustean analysis. Changes in environmental conditions were mainly marked by an improvement in water quality between 1985 and 1991 and by an increase in water temperature from 1985 onwards due to climate change. Improvement in water quality seemed to delay changes in community structures under global warming. We then observed trends in community structures coupled with high temperatures and a decrease in oxygen content. Interestingly, we observed both gradual changes and rapid switches in community states. These shifts seemed coupled to extreme hydroclimatic events (i.e. pulse disturbances). Floods and the 2003 heatwave enhanced the development of eurytolerant and invasive taxa which were probably able to take advantage of gradual warming environmental conditions. Despite various site-specific "press" constraints (e.g. hydropower schemes, nuclear power plants), similar changes in community structures were observed along the French Rhône River. Such consistency in temporal processes at large geographical scales underlined the strength of hydroclimatic constraints on community dynamics compared to specific local disturbances. Finally, community structures did not show any sign of recovery, and their relative sensitivities to extreme hydroclimatic events seemed to increase with time. Thus, our results suggest that global changes may reduce the resilience of current community states.