Body size and trophic position determine the outcomes of species invasions along temperature and productivity gradients.

Species invasions are predicted to increase in frequency with global change, but quantitative predictions of how environmental filters and species traits influence the success and consequences of invasions for local communities are lacking. Here we investigate how invaders alter the structure, diversity and stability regime of simple communities across environmental gradients (habitat productivity, temperature) and community size structure. We simulate all three-species trophic modules (apparent and exploitative competition, trophic chain and intraguild predation). We predict that invasions most often succeed in warm and productive habitats and that successful invaders include smaller competitors, intraguild predators and comparatively small top predators. This suggests that species invasions and global change may facilitate the downsizing of food webs. Furthermore, we show that successful invasions leading to species substitutions rarely alter system stability, while invasions leading to increased diversity can destabilize or stabilize community dynamics depending on the environmental conditions and invader's trophic position.

Changes in vertical and horizontal diversities mediated by the size structure of introduced fish collectively shape food-web stability.

Species introductions can alter local food-web structure by changing the vertical or horizontal diversity within communities, largely driven by their body size distributions. Increasing vertical and horizontal diversities is predicted to have opposing effects on stability. However, their interactive effects remain largely overlooked. We investigated the independent and collective effects of vertical and horizontal diversities on food-web stability in alpine lakes stocked with variable body size distributions of introduced fish species. Introduced predators destabilize food-webs by increasing vertical diversity through food chain lengthening. Alternatively, increasing horizontal diversity results in more stable food-web topologies. A non-linear interaction between vertical and horizontal diversities suggests that increasing vertical diversity is most destabilizing when horizontal diversity is low. Our findings suggest that the size structure of introduced predators drives their impacts on stability by modifying the structure of food-webs, and highlights the interactive effects of vertical and horizontal diversities on stability.

Rapid evolution of unimodal but not of linear thermal performance curves in Daphnia magna.

Species may cope with warming through both rapid evolutionary and plastic responses. While thermal performance curves (TPCs), reflecting thermal plasticity, are considered powerful tools to understand the impact of warming on ectotherms, their rapid evolution has been rarely studied for multiple traits. We capitalized on a 2-year experimental evolution trial in outdoor mesocosms that were kept at ambient temperatures or heated 4°C above ambient, by testing in a follow-up common-garden experiment, for rapid evolution of the TPCs for multiple key traits of the water flea Daphnia magna. The heat-selected Daphnia showed evolutionary shifts of the unimodal TPCs for survival, fecundity at first clutch and intrinsic population growth rate toward higher optimum temperatures, and a less pronounced downward curvature indicating a better ability to keep fitness high across a range of high temperatures. We detected no evolution of the linear TPCs for somatic growth, mass and development rate, and for the traits related to energy gain (ingestion rate) and costs (metabolic rate). As a result, also the relative thermal slope of energy gain versus energy costs did not vary. These results suggest the overall (rather than per capita) top-down impact of D. magna may increase under rapid thermal evolution.

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.

A roadmap for ladybird conservation and recovery.

Ladybirds (Coleoptera: Coccinellidae) provide services that are critical to food production, and they fulfill an ecological role as a food source for predators. The richness, abundance, and distribution of ladybirds, however, are compromised by many anthropogenic threats. Meanwhile, a lack of knowledge of the conservation status of most species and the factors driving their population dynamics hinders the development and implementation of conservation strategies for ladybirds. We conducted a review of the literature on the ecology, diversity, and conservation of ladybirds to identify their key ecological threats. Ladybird populations are most affected by climate factors, landscape composition, and biological invasions. We suggest mitigating actions for ladybird conservation and recovery. Short-term actions include citizen science programs and education, protective measures for habitat recovery and threatened species, prevention of the introduction of non-native species, and the maintenance and restoration of natural areas and landscape heterogeneity. Mid-term actions involve the analysis of data from monitoring programs and insect collections to disentangle the effect of different threats to ladybird populations, understand habitat use by taxa on which there is limited knowledge, and quantify temporal trends of abundance, diversity, and biomass along a management-intensity gradient. Long-term actions include the development of a worldwide monitoring program based on standardized sampling to fill data gaps, increase explanatory power, streamline analyses, and facilitate global collaborations.

Las catarinas (Coleoptera: Coccinellidae) proporcionan servicios que son críticos para la producción de alimento, y juegan un papel ecológico como fuente de alimento para depredadores. Sin embargo, la riqueza, abundancia y distribución de catarinas están en peligro debido a muchas amenazas antropogénicas. La carencia de conocimiento sobre el estatus de conservación de la mayoría de las especies y los factores que inciden en su dinámica poblacional dificulta el desarrollo e implementación de estrategias de conservación para las catarinas. Realizamos una revisión de la literatura sobre la ecología, diversidad y conservación de catarinas para identificar sus amenazas ecológicas clave. Las poblaciones de catarinas fueron afectadas mayormente por factores climáticos, composición del paisaje e invasiones biológicas. Proponemos acciones de mitigación para la conservación y recuperación de catarinas. Acciones a corto plazo incluyen programas de ciencia y educación ciudadana, medidas de protección para la recuperación de hábitat y de especies amenazadas, prevención de la introducción de especies no nativas y el mantenimiento y restauración de áreas naturales y la heterogeneidad del paisaje. Acciones a mediano plazo implican el análisis de datos obtenidos de programas de monitoreo y colecciones de insectos para desenmarañar el efecto de las diferentes amenazas a las poblaciones de catarinas, comprender el uso del hábitat por taxa de los que se tiene conocimiento limitado y cuantifica las tendencias temporales de la abundancia, diversidad y biomasa a lo largo de un gradiente de intensidad de manejo. Acciones a largo plazo incluyen el desarrollo de un programa de monitoreo a nivel mundial basado en muestreos estandarizados para subsanar la falta de datos, incrementar el poder explicativo, optimizar los análisis y facilitar colaboraciones globales.

Energetic mismatch induced by warming decreases leaf litter decomposition by aquatic detritivores.

The balance of energetic losses and gains is of paramount importance for understanding and predicting the persistence of populations and ecosystem processes in a rapidly changing world. Previous studies suggested that metabolic rate often increases faster with warming than resource ingestion rate, leading to an energetic mismatch at high temperature. However, little is known about the ecological consequences of this energetic mismatch for population demography and ecosystem functions. Here, we combined laboratory experiments and modelling to investigate the energetic balance of a stream detritivore Gammarus fossarum along a temperature gradient and the consequences for detritivore populations and organic matter decomposition. We experimentally measured the energetic losses (metabolic rate) and supplies (ingestion rate) of Gammarus and we modelled the impact of rising temperatures and changes in Gammarus body size induced by warming on population dynamics and benthic organic matter dynamics in freshwater systems. Our experimental results indicated an energetic mismatch in a Gammarus population where losses via metabolic rate increase faster than supplies via food ingestion with warming, which translated in a decrease in energetic efficiency with temperature rising from 5 to 20°C. Moreover, our consumer-resource model predicts a decrease in the biomass of Gammarus population with warming, associated with lower maximum abundances and steeper abundance decreases after biomass annual peaks. These changes resulted in a decrease in leaf litter decomposition rate and thus longer persistence of leaf litter standing stock over years in the simulations. In addition, Gammarus body size reductions led to shorter persistence for both leaf litter and Gammarus biomasses at low temperature and the opposite trend at high temperature, revealing that body size reduction was weakening the effect of temperature on resource and consumer persistence. Our model contributes to identifying the mechanisms that explain how thermal effects at the level of individuals may cascade through trophic interactions and influence important ecosystem processes. Considering the balance of physiological processes is crucial to improve our ability to predict the impact of climate change on carbon stocks and ecosystem functions.

Thermal plasticity and evolution shape predator-prey interactions differently in clear and turbid water bodies.

Warming and eutrophication negatively affect freshwater ecosystems by modifying trophic interactions and increasing water turbidity. We need to consider their joint effects on predator-prey interactions and how these depend on the thermal evolution of both predator and prey. We quantified how 4°C warming and algae-induced turbidity (that integrates turbidity per se and increased food for zooplankton prey) affect functional response parameters and prey population parameters in a common-garden experiment. We did so for all combinations of high- and low-latitude predator (damselfly larvae) and prey (water fleas) populations to assess the potential impact of thermal evolution of predators and/or prey at a high latitude under warming using a space-for-time substitution. We then modelled effects on the system stability (i.e. tendency to oscillate) under different warming, turbidity and evolutionary scenarios. Warming and turbidity had little effect on the functional response parameters of high-latitude predators. In contrast, warming and turbidity reduced the handling times of low-latitude predators. Moreover, warming increased the search rates of low-latitude predators in clear water but instead decreased these in turbid water. Warming increased stability (i.e. prevented oscillations) in turbid water (except for the 'high-latitude predator and high-latitude prey' system), mainly by decreasing the prey's carrying capacity and partly also by decreasing search rates, while it did not affect stability in clear water. Algae-induced turbidity generally decreased stability, mainly by increasing the prey's carrying capacity and partly also by increasing search rates. This resembles findings that nutrient enrichment can reduce the stability of trophic systems. The expected stability of the high-latitude trophic system under warming was dependent on the turbidity level: our results suggest that thermal plasticity tends to destabilize the high-latitude trophic system under warming in clear water but not in turbid water, and that thermal evolution of the predator will stabilize the high-latitude system under warming in turbid water but less so in clear water. The extent to which thermal plasticity and evolution shape trophic system stability under warming may strongly differ between clear and turbid water bodies, with their contributions having a more stabilizing role in turbid water.

Cryptic eco-evolutionary feedback in the city: Urban evolution of prey dampens the effect of urban evolution of the predator.

Most research on eco-evolutionary feedbacks focuses on ecological consequences of evolution in a single species. This ignores the fact that evolution in response to a shared environmental factor in multiple species involved in interactions could alter the net cumulative effect of evolution on ecology. We empirically tested whether urbanization-driven evolution in a predator (nymphs of the damselfly Ischnura elegans) and its prey (the water flea Daphnia magna) jointly shape the outcome of predation under simulated heatwaves. Both interactors show genetic trait adaptation to urbanization, particularly to higher temperatures. We cross-exposed common-garden reared damselflies and Daphnia from replicated urban and rural populations, and quantified predation rates and functional response traits. Urban damselfly nymphs showed higher encounter and predation rates than rural damselflies when exposed to rural prey, but this difference disappeared when they preyed on urban Daphnia. This represents a case of a cryptic evo-to-eco feedback, where the evolution of one species dampens the effects of the evolution of another species on their interaction strength. The effects of evolution of each single species were strong: the scenario in which only the predator or prey was adapted to urbanization resulted in a c. 250% increase in encounter rate and a c. 25% increase in predation rate, compared to the rural predator-rural prey combination. Our results provide unique evidence for eco-evolutionary feedbacks in cities, and underscore the importance of a multi-species approach in eco-evolutionary dynamics research.

Theory of temperature-dependent consumer-resource interactions.

Changes in temperature affect consumer-resource interactions, which underpin the functioning of ecosystems. However, existing studies report contrasting predictions regarding the impacts of warming on biological rates and community dynamics. To improve prediction accuracy and comparability, we develop an approach that combines sensitivity analysis and aggregate parameters. The former determines which biological parameters impact the community most strongly. The use of aggregate parameters (i.e., maximal energetic efficiency, ρ, and interaction strength, κ), that combine multiple biological parameters, increases explanatory power and reduces the complexity of theoretical analyses. We illustrate the approach using empirically derived thermal dependence curves of biological rates and applying it to consumer-resource biomass ratio and community stability. Based on our analyses, we generate four predictions: (1) resource growth rate regulates biomass distributions at mild temperatures, (2) interaction strength alone determines the thermal boundaries of the community, (3) warming destabilises dynamics at low and mild temperatures only and (4) interactions strength must decrease faster than maximal energetic efficiency for warming to stabilise dynamics. We argue for the potential benefits of directly working with the aggregate parameters to increase the accuracy of predictions on warming impacts on food webs and promote cross-system comparisons.

Warming indirectly increases invasion success in food webs.

Climate warming and biological invasions are key drivers of biodiversity change. Their combined effects on ecological communities remain largely unexplored. We investigated the direct and indirect influences of temperature on invasion success, and their synergistic effects on community structure and dynamics. Using size-structured food web models, we found that higher temperatures increased invasion success. The direct physiological effects of temperature on invasions were minimal in comparison with indirect effects mediated by changes on food web structure and stability. Warmer communities with less connectivity, shortened food chains and reduced temporal variability were more susceptible to invasions. The directionality and magnitude of invasions effects on food webs varied across temperature regimes. When invaded, warmer communities became smaller, more connected and with more predator species than their colder counterparts. They were also less stable and their species more abundant. Considering food web structure is crucial to predict invasion success and its impacts along temperature gradients.

Thermal mismatches in biological rates determine trophic control and biomass distribution under warming.

Temperature has numerous effects on the structure and dynamics of ecological communities. Yet, there is no general trend or consensus on the magnitude and directions of these effects. To fill this gap, we propose a mechanistic framework based on key biological rates that predicts how temperature influences biomass distribution and trophic control in food webs. We show that these predictions arise from thermal mismatches between biological rates and across trophic levels. We couple our theory with experimental data for a wide range of species and find that warming should lead to top-heavier terrestrial food chains and stronger top-down control in aquatic environments. We then derive predictions for the effects of temperature on herbivory and validate them with data on stream grazers. Our study provides a mechanistic explanation of thermal effects on consumer-resource systems which is crucial to better understand the biogeography and the consequences of global warming on trophic dynamics.

Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades.

Trophic cascades - the indirect effect of predators on non-adjacent lower trophic levels - are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences trophic cascade strength in a terrestrial tri-trophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores' lineage and host-plant specialization but are not associated with density-dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of trophic cascade strength and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi-trophic interactions.

Tri-trophic interactions: bridging species, communities and ecosystems.

A vast body of research demonstrates that many ecological and evolutionary processes can only be understood from a tri-trophic viewpoint, that is, one that moves beyond the pairwise interactions of neighbouring trophic levels to consider the emergent features of interactions among multiple trophic levels. Despite its unifying potential, tri-trophic research has been fragmented, following two distinct paths. One has focused on the population biology and evolutionary ecology of simple food chains of interacting species. The other has focused on bottom-up and top-down controls over the distribution of biomass across trophic levels and other ecosystem-level variables. Here, we propose pathways to bridge these two long-standing perspectives. We argue that an expanded theory of tri-trophic interactions (TTIs) can unify our understanding of biological processes across scales and levels of organisation, ranging from species evolution and pairwise interactions to community structure and ecosystem function. To do so requires addressing how community structure and ecosystem function arise as emergent properties of component TTIs, and, in turn, how species traits and TTIs are shaped by the ecosystem processes and the abiotic environment in which they are embedded. We conclude that novel insights will come from applying tri-trophic theory systematically across all levels of biological organisation.

Evolution without standing genetic variation: change in transgenerational plastic response under persistent predation pressure.

Transgenerational phenotypic plasticity is a fast non-genetic response to environmental modifications that can buffer the effects of environmental stresses on populations. However, little is known about the evolution of plasticity in the absence of standing genetic variation although several non-genetic inheritance mechanisms have now been identified. Here we monitored the pea aphid transgenerational phenotypic response to ladybird predators (production of winged offspring) during 27 generations of experimental evolution in the absence of initial genetic variation (clonal multiplication starting from a single individual). We found that the frequency of winged aphids first increased rapidly in response to predators and then remained stable over 25 generations, implying a stable phenotypic reconstruction at each generation. We also found that the high frequency of winged aphids persisted for one generation after removing predators. Winged aphid frequency then entered a refractory phase during which it dropped below the level of control lines for at least two generations before returning to it. Interestingly, the persistence of the winged phenotype decreased and the refractory phase lasted longer with the increasing number of generations of exposure to predators. Finally, we found that aphids continuously exposed to predators for 22 generations evolved a significantly weaker plastic response than aphids never exposed to predators, which, in turn, increased their fitness in presence of predators. Our findings therefore showcased an example of experimental evolution of plasticity in the absence of initial genetic variation and highlight the importance of integrating several components of non-genetic inheritance to detect evolutionary responses to environmental changes.

Temperature-size responses alter food chain persistence across environmental gradients.

Body-size reduction is a ubiquitous response to global warming alongside changes in species phenology and distributions. However, ecological consequences of temperature-size (TS) responses for community persistence under environmental change remain largely unexplored. Here, we investigated the interactive effects of warming, enrichment, community size structure and TS responses on a three-species food chain using a temperature-dependent model with empirical parameterisation. We found that TS responses often increase community persistence, mainly by modifying consumer-resource size ratios and thereby altering interaction strengths and energetic efficiencies. However, the sign and magnitude of these effects vary with warming and enrichment levels, TS responses of constituent species, and community size structure. We predict that the consequences of TS responses are stronger in aquatic than in terrestrial ecosystems, especially when species show different TS responses. We conclude that considering the links between phenotypic plasticity, environmental drivers and species interactions is crucial to better predict global change impacts on ecosystem diversity and stability.

Non-additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity.

Understanding the effects of extreme climatic events on species and their interactions is of paramount importance for predicting and mitigating the impacts of climate change on communities and ecosystems. However, the joint effects of extreme climatic events and species interactions on the behaviour and phenotype of organisms remain poorly understood, leaving a substantial gap in our knowledge on the impacts of climatic change on ecological communities. Using an aphid-ladybeetle system, we experimentally investigated the effects of predators and heat shocks on prey body size, microhabitat use, and transgenerational phenotypic plasticity (i.e., the asexual production of winged offspring by unwinged mothers). We found that (i) aphids were smaller in the presence of predators but larger when exposed to frequent heat shocks; (ii) frequent heat shocks shifted aphid distribution towards the plant's apex, but the presence of predators had the opposite effect and dampened the heat-shock effects; and (iii) aphids responded to predators by producing winged offspring, but heat shocks strongly inhibited this transgenerational response to predation. Overall, our experimental results show that heat shocks inhibit phenotypic and behavioural responses to predation (and vice versa) and that such changes may alter trophic interactions, and have important consequences on the dynamics and stability of ecological communities. We conclude that the effects of extreme climatic events on the phenotype and behaviour of interacting species should be considered to understand the effects of climate change on species interactions and communities.

Predator diversity and environmental change modify the strengths of trophic and nontrophic interactions.

Understanding the dependence of species interaction strengths on environmental factors and species diversity is crucial to predict community dynamics and persistence in a rapidly changing world. Nontrophic (e.g. predator interference) and trophic components together determine species interaction strengths, but the effects of environmental factors on these two components remain largely unknown. This impedes our ability to fully understand the links between environmental drivers and species interactions. Here, we used a dynamical modelling framework based on measured predator functional responses to investigate the effects of predator diversity, prey density, and temperature on trophic and nontrophic interaction strengths within a freshwater food web. We found that (i) species interaction strengths cannot be predicted from trophic interactions alone, (ii) nontrophic interaction strengths vary strongly among predator assemblages, (iii) temperature has opposite effects on trophic and nontrophic interaction strengths, and (iv) trophic interaction strengths decrease with prey density, whereas the dependence of nontrophic interaction strengths on prey density is concave up. Interestingly, the qualitative impacts of temperature and prey density on the strengths of trophic and nontrophic interactions were independent of predator identity, suggesting a general pattern. Our results indicate that taking multiple environmental factors and the nonlinearity of density-dependent species interactions into account is an important step towards a better understanding of the effects of environmental variations on complex ecological communities. The functional response approach used in this study opens new avenues for (i) the quantification of the relative importance of the trophic and nontrophic components in species interactions and (ii) a better understanding how environmental factors affect these interactions and the dynamics of ecological communities.

The smell of change: warming affects species interactions mediated by chemical information.

Knowledge of how temperature influences an organism's physiology and behaviour is of paramount importance for understanding and predicting the impacts of climate change on species' interactions. While the behaviour of many organisms is driven by chemical information on which they rely on to detect resources, conspecifics, natural enemies and competitors, the effects of temperature on infochemical-mediated interactions remain largely unexplored. Here, we experimentally show that temperature strongly influences the emission of infochemicals by ladybeetle larvae, which, in turn, modifies the oviposition behaviour of conspecific females. Temperature also directly affects female perception of infochemicals and their oviposition behaviour. Our results suggest that temperature-mediated effects on chemical communication can influence flows across system boundaries (e.g. immigration and emigration) and thus alter the dynamics and stability of ecological networks. We therefore argue that investigating the effects of temperature on chemical communication is a crucial step towards a better understanding of the functioning of ecological communities facing rapid environmental changes.

Thermal acclimation modulates the impacts of temperature and enrichment on trophic interaction strengths and population dynamics.

Global change affects individual phenotypes and biotic interactions, which can have cascading effects up to the ecosystem level. However, the role of environmentally induced phenotypic plasticity in species interactions is poorly understood, leaving a substantial gap in our knowledge of the impacts of global change on ecosystems. Using a cladoceran-dragonfly system, we experimentally investigated the effects of thermal acclimation, acute temperature change and enrichment on predator functional response and metabolic rate. Using our experimental data, we next parameterized a population dynamics model to determine the consequences of these effects on trophic interaction strength and food-chain stability. We found that (1) predation and metabolic rates of the dragonfly larvae increase with acute warming, (2) warm-acclimated larvae have a higher maximum predation rate than cold-acclimated ones, and (3) long-term interaction strength increases with enrichment but decreases with both acclimation and acute temperatures. Overall, our experimental results show that thermal acclimation can buffer negative impacts of environmental change on predators and increase food-web stability and persistence. We conclude that the effect of acclimation and, more generally, phenotypic plasticity on trophic interactions should not be overlooked if we aim to understand the effects of climate change and enrichment on species interaction strength and food-web stability.

Towards a mechanistic understanding of temperature and enrichment effects on species interaction strength, omnivory and food-web structure.

Revealing the links between species functional traits, interaction strength and food-web structure is of paramount importance for understanding and predicting the relationships between food-web diversity and stability in a rapidly changing world. However, little is known about the interactive effects of environmental perturbations on individual species, trophic interactions and ecosystem functioning. Here, we combined modelling and laboratory experiments to investigate the effects of warming and enrichment on a terrestrial tritrophic system. We found that the food-web structure is highly variable and switches between exploitative competition and omnivory depending on the effects of temperature and enrichment on foraging behaviour and species interaction strength. Our model contributes to identifying the mechanisms that explain how environmental effects cascade through the food web and influence its topology. We conclude that considering environmental factors and flexible food-web structure is crucial to improve our ability to predict the impacts of global changes on ecosystem diversity and stability.