Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functions.

Loss in intraspecific diversity can alter ecosystem functions, but the underlying mechanisms are still elusive, and intraspecific biodiversity-ecosystem function (iBEF) relationships have been restrained to primary producers. Here, we manipulated genetic and functional richness of a fish consumer (Phoxinus phoxinus) to test whether iBEF relationships exist in consumer species and whether they are more likely sustained by genetic or functional richness. We found that both genotypic and functional richness affected ecosystem functioning, either independently or interactively. Loss in genotypic richness reduced benthic invertebrate diversity consistently across functional richness treatments, whereas it reduced zooplankton diversity only when functional richness was high. Finally, losses in genotypic and functional richness altered functions (decomposition) through trophic cascades. We concluded that iBEF relationships lead to substantial top-down effects on entire food chains. The loss of genotypic richness impacted ecological properties as much as the loss of functional richness, probably because it sustains "cryptic" functional diversity.

Phytoplankton biodiversity is more important for ecosystem functioning in highly variable thermal environments.

The 21st century has seen an acceleration of anthropogenic climate change and biodiversity loss, with both stressors deemed to affect ecosystem functioning. However, we know little about the interactive effects of both stressors and in particular about the interaction of increased climatic variability and biodiversity loss on ecosystem functioning. This should be remedied because larger climatic variability is one of the main features of climate change. Here, we demonstrated that temperature fluctuations led to changes in the importance of biodiversity for ecosystem functioning. We used microcosm communities of different phytoplankton species richness and exposed them to a constant, mild, and severe temperature-fluctuating environment. Wider temperature fluctuations led to steeper biodiversity-ecosystem functioning slopes, meaning that species loss had a stronger negative effect on ecosystem functioning in more fluctuating environments. For severe temperature fluctuations, the slope increased through time due to a decrease of the productivity of species-poor communities over time. We developed a theoretical competition model to better understand our experimental results and showed that larger differences in thermal tolerances across species led to steeper biodiversity-ecosystem functioning slopes. Species-rich communities maintained their ecosystem functioning with increased fluctuation as they contained species able to resist the thermally fluctuating environments, while this was on average not the case in species-poor communities. Our results highlight the importance of biodiversity for maintaining ecosystem functions and services in the context of increased climatic variability under climate change.

Predicting effects of multiple interacting global change drivers across trophic levels.

Global change encompasses many co-occurring anthropogenic drivers, which can act synergistically or antagonistically on ecological systems. Predicting how different global change drivers simultaneously contribute to observed biodiversity change is a key challenge for ecology and conservation. However, we lack the mechanistic understanding of how multiple global change drivers influence the vital rates of multiple interacting species. We propose that reaction norms, the relationships between a driver and vital rates like growth, mortality, and consumption, provide insights to the underlying mechanisms of community responses to multiple drivers. Understanding how multiple drivers interact to affect demographic rates using a reaction-norm perspective can improve our ability to make predictions of interactions at higher levels of organization-that is, community and food web. Building on the framework of consumer-resource interactions and widely studied thermal performance curves, we illustrate how joint driver impacts can be scaled up from the population to the community level. A simple proof-of-concept model demonstrates how reaction norms of vital rates predict the prevalence of driver interactions at the community level. A literature search suggests that our proposed approach is not yet used in multiple driver research. We outline how realistic response surfaces (i.e., multidimensional reaction norms) can be inferred by parametric and nonparametric approaches. Response surfaces have the potential to strengthen our understanding of how multiple drivers affect communities as well as improve our ability to predict when interactive effects emerge, two of the major challenges of ecology today.

Treated and highly diluted, but wastewater still impacts diversity and energy fluxes of freshwater food webs.

Wastewater treatment plants (WWTPs) have greatly improved water quality globally. However, treated effluents still contain a complex cocktail of pollutants whose environmental effects might go unnoticed, masked by additional stressors in the receiving waters or by spatiotemporal variability. We conducted a BACI (Before-After/Control-Impact) ecosystem manipulation experiment, where we diverted part of the effluent of a large tertiary WWTP into a small, unpolluted stream to assess the effects of a well-treated and highly diluted effluent on riverine diversity and food web dynamics. We sampled basal food resources, benthic invertebrates and fish to search for changes on the structure and energy transfer of the food web with the effluent. Although effluent toxicity was low, it reduced diversity, increased primary production and herbivory, and reduced energy fluxes associated to terrestrial inputs. Altogether, the effluent decreased total energy fluxes in stream food webs, showing that treated wastewater can lead to important ecosystem-level changes, affecting the structure and functioning of stream communities even at high dilution rates. The present study shows that current procedures to treat wastewater can still affect freshwater ecosystems and highlights the need for further efforts to treat polluted waters to conserve aquatic food webs.

Water diversion and pollution interactively shape freshwater food webs through bottom-up mechanisms.

Water diversion and pollution are two pervasive stressors in river ecosystems that often co-occur. Individual effects of both stressors on basal resources available to stream communities have been described, with diversion reducing detritus standing stocks and pollution increasing biomass of primary producers. However, interactive effects of both stressors on the structure and trophic basis of food webs remain unknown. We hypothesized that the interaction between both stressors increases the contribution of the green pathway in stream food webs. Given the key role of the high-quality, but less abundant, primary producers, we also hypothesized an increase in food web complexity with larger trophic diversity in the presence of water diversion and pollution. To test these hypotheses, we selected four rivers in a range of pollution subject to similar water diversion schemes, and we compared food webs upstream and downstream of the diversion. We characterized food webs by means of stable isotope analysis. Both stressors directly changed the availability of basal resources, with water diversion affecting the brown food web by decreasing detritus stocks, and pollution enhancing the green food web by promoting biofilm production. The propagation of the effects at the base of the food web to higher trophic levels differed between stressors. Water diversion had little effect on the structure of food webs, but pollution increased food chain length and trophic diversity, and reduced trophic redundancy. The effects at higher trophic levels were exacerbated when combining both stressors, as the relative contribution of biofilm to the stock of basal resources increased even further. Overall, we conclude that moderate pollution increases food web complexity and that the interaction with water abstraction seems to amplify this effect. Our study shows the importance of assessing the interaction between stressors to create predictive tools for a proper management of ecosystems.

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.

The impact of climate warming on species diversity across scales: Lessons from experimental meta-ecosystems.

Aim: The aim was to evaluate the effects of climate warming on biodiversity across spatial scales (i.e., α-, ß- and γ-diversity) and the effects of patch openness and experimental context on diversity responses. Location: Global. Time period: 1995-2017. Major taxa studied: Fungi, invertebrates, phytoplankton, plants, seaweed, soil microbes and zooplankton. Methods: We compiled data from warming experiments and conducted a meta-analysis to evaluate the effects of warming on different components of diversity (such as species richness and equivalent numbers) at different spatial scales (α-, ß- and γ-diversity, partitioning ß-diversity into species turnover and nestedness components). We also investigated how these effects were modulated by system openness, defined as the possibility of replicates being colonized by new species, and experimental context (duration, mean temperature change and ecosystem type). Results: Experimental warming did not affect local species richness (α-diversity) but decreased effective numbers of species by affecting species dominance. Warming increased species spatial turnover (ß-diversity), although no significant changes were detected at the regional scale (γ-diversity). Site openness and experimental context did not significantly affect our results, despite significant heterogeneity in the effect sizes of α- and ß-diversity. Main conclusions: Our meta-analysis shows that the effects of warming on biodiversity are scale dependent. The local and regional inventory diversity remain unaltered, whereas species composition across temperature gradients and the patterns of species dominance change with temperature, creating novel communities that might be harder to predict.

The spatial scaling of food web structure across European biogeographical regions.

The species-area relationship (SAR) is one of the most well-established scaling patterns in ecology. Its implications for understanding how communities change across spatial gradients are numerous, including the effects of habitat loss on biodiversity. However, ecological communities are not mere collections of species. They are the result of interactions between these species forming complex networks that tie them together. Should we aim to grasp the spatial scaling of biodiversity as a whole, it is fundamental to understand the changes in the structure of interaction networks with area. In spite of a few empirical and theoretical studies that address this challenge, we still do not know much about how network structure changes with area, or what are the main environmental drivers of these changes. Here, using the meta-network of potential interactions between all terrestrial vertebrates in Europe (1140 species and 67 201 feeding interactions), we analysed network-area relationships (NARs) that summarize how network properties scale with area. We do this across ten biogeographical regions, which differ in environmental characteristics. We found that the spatial scaling of network complexity strongly varied across biogeographical regions. However, once the variation in SARs was accounted for, differences in the shape of NARs vanished. On the other hand, the proportion of species across trophic levels remained remarkably constant across biogeographical regions and spatial scales, despite the great variation in species richness. Spatial variation in mean annual temperature and habitat clustering were the main environmental determinants of the shape of both SARs and NARs across Europe. Our results suggest new avenues in the exploration of the effects of environmental factors on the spatial scaling of biodiversity. We argue that NARs can provide new insights to analyse and understand ecological communities.

Assessing the strength and sensitivity of the core microbiota approach on a highly diverse sponge reef.

Marine sponge reefs usually comprise a complex array of taxonomically different sponge species, many of these hosting highly diverse microbial communities. The number of microbial species known to occupy a given sponge ranges from tens to thousands, bringing numerous challenges to their analysis. One way to deal with such complexity is to use a core microbiota approach, in which only prevalent and abundant microbes are considered. Here we aimed to test the strength and sensitivity of the core microbiota approach by applying different core definitions to 20 host sponge species. Application of increasingly stringent relative abundance and/or percentage occurrence thresholds to qualify as part of the core microbiota decreased the number of 'core' OTUs and phyla and, consequently, changed both alpha- and beta-diversity patterns. Moreover, microbial co-occurrence patterns explored using correlation networks were also affected by the core microbiota definition. The application of stricter thresholds resulted in smaller and less compartmentalized networks, with different keystone species. These results highlight that the application of different core definitions to phylogenetically disparate host species can result in the drawing of markedly different conclusions. Consequently, we recommend to assess the effects of different core community definitions on the specific system of study before considering its application.

The geographical variation of network structure is scale dependent: understanding the biotic specialization of host-parasitoid networks.

Research on the structure of ecological networks suggests that a number of universal patterns exist. Historically, biotic specialization has been thought to increase towards the Equator. Yet, recent studies have challenged this view showing non-conclusive results. Most studies analysing the geographical variation in biotic specialization focus, however, only on the local scale. Little is known about how the geographical variation of network structure depends on the spatial scale of observation (i.e., from local to regional spatial scales). This should be remedied, as network structure changes as the spatial scale of observation changes, and the magnitude and shape of these changes can elucidate the mechanisms behind the geographical variation in biotic specialization. Here we analyse four facets of biotic specialization in host-parasitoid networks along gradients of climatic constancy, classifying the networks according to their spatial extension (local or regional). Namely, we analyse network connectance, consumer diet overlap, consumer diet breadth, and resource vulnerability at both local and regional scales along the gradients of both current climatic constancy and historical climatic change. While at the regional scale none of the climatic variables are associated to biotic specialization, at the local scale, network connectance, consumer diet overlap, and resource vulnerability decrease with current climatic constancy, whereas consumer generalism increases (i.e., broader diet breadths in tropical areas). Similar patterns are observed along the gradient of historical climatic change. We provide an explanation based on different beta-diversity for consumers and resources across the geographical gradients. Our results show that the geographical gradient of biotic specialization is not universal. It depends on both the facet of biotic specialization and the spatial scale of observation.

Uncovering the drivers of host-associated microbiota with joint species distribution modelling.

In addition to the processes structuring free-living communities, host-associated microbiota are directly or indirectly shaped by the host. Therefore, microbiota data have a hierarchical structure where samples are nested under one or several variables representing host-specific factors, often spanning multiple levels of biological organization. Current statistical methods do not accommodate this hierarchical data structure and therefore cannot explicitly account for the effect of the host in structuring the microbiota. We introduce a novel extension of joint species distribution models (JSDMs) which can straightforwardly accommodate and discern between effects such as host phylogeny and traits, recorded covariates such as diet and collection site, among other ecological processes. Our proposed methodology includes powerful yet familiar outputs seen in community ecology overall, including (a) model-based ordination to visualize and quantify the main patterns in the data; (b) variance partitioning to assess how influential the included host-specific factors are in structuring the microbiota; and (c) co-occurrence networks to visualize microbe-to-microbe associations.

Five Years of Experimental Warming Increases the Biodiversity and Productivity of Phytoplankton.

Phytoplankton are key components of aquatic ecosystems, fixing CO2 from the atmosphere through photosynthesis and supporting secondary production, yet relatively little is known about how future global warming might alter their biodiversity and associated ecosystem functioning. Here, we explore how the structure, function, and biodiversity of a planktonic metacommunity was altered after five years of experimental warming. Our outdoor mesocosm experiment was open to natural dispersal from the regional species pool, allowing us to explore the effects of experimental warming in the context of metacommunity dynamics. Warming of 4°C led to a 67% increase in the species richness of the phytoplankton, more evenly-distributed abundance, and higher rates of gross primary productivity. Warming elevated productivity indirectly, by increasing the biodiversity and biomass of the local phytoplankton communities. Warming also systematically shifted the taxonomic and functional trait composition of the phytoplankton, favoring large, colonial, inedible phytoplankton taxa, suggesting stronger top-down control, mediated by zooplankton grazing played an important role. Overall, our findings suggest that temperature can modulate species coexistence, and through such mechanisms, global warming could, in some cases, increase the species richness and productivity of phytoplankton communities.

Reconciling the temperature dependence of respiration across timescales and ecosystem types.

Ecosystem respiration is the biotic conversion of organic carbon to carbon dioxide by all of the organisms in an ecosystem, including both consumers and primary producers. Respiration exhibits an exponential temperature dependence at the subcellular and individual levels, but at the ecosystem level respiration can be modified by many variables including community abundance and biomass, which vary substantially among ecosystems. Despite its importance for predicting the responses of the biosphere to climate change, it is as yet unknown whether the temperature dependence of ecosystem respiration varies systematically between aquatic and terrestrial environments. Here we use the largest database of respiratory measurements yet compiled to show that the sensitivity of ecosystem respiration to seasonal changes in temperature is remarkably similar for diverse environments encompassing lakes, rivers, estuaries, the open ocean and forested and non-forested terrestrial ecosystems, with an average activation energy similar to that of the respiratory complex (approximately 0.65 electronvolts (eV)). By contrast, annual ecosystem respiration shows a substantially greater temperature dependence across aquatic (approximately 0.65 eV) versus terrestrial ecosystems (approximately 0.32 eV) that span broad geographic gradients in temperature. Using a model derived from metabolic theory, these findings can be reconciled by similarities in the biochemical kinetics of metabolism at the subcellular level, and fundamental differences in the importance of other variables besides temperature­such as primary productivity and allochthonous carbon inputs­on the structure of aquatic and terrestrial biota at the community level.

Evaluating the core microbiota in complex communities: A systematic investigation.

The study of complex microbial communities poses unique conceptual and analytical challenges, with microbial species potentially numbering in the thousands. With transient or allochthonous microorganisms often adding to this complexity, a 'core' microbiota approach, focusing only on the stable and permanent members of the community, is becoming increasingly popular. Given the various ways of defining a core microbiota, it is prudent to examine whether the definition of the core impacts upon the results obtained. Here we used complex marine sponge microbiotas and undertook a systematic evaluation of the degree to which different factors used to define the core influenced the conclusions. Significant differences in alpha- and beta-diversity were detected using some but not all core definitions. However, findings related to host specificity and environmental quality were largely insensitive to major changes in the core microbiota definition. Furthermore, none of the applied definitions altered our perception of the ecological networks summarising interactions among bacteria within the sponges. These results suggest that, while care should still be taken in interpretation, the core microbiota approach is surprisingly robust, at least for comparing microbiotas of closely related samples.

Navigating the complexity of ecological stability.

Human actions challenge nature in many ways. Ecological responses are ineluctably complex, demanding measures that describe them succinctly. Collectively, these measures encapsulate the overall 'stability' of the system. Many international bodies, including the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, broadly aspire to maintain or enhance ecological stability. Such bodies frequently use terms pertaining to stability that lack clear definition. Consequently, we cannot measure them and so they disconnect from a large body of theoretical and empirical understanding. We assess the scientific and policy literature and show that this disconnect is one consequence of an inconsistent and one-dimensional approach that ecologists have taken to both disturbances and stability. This has led to confused communication of the nature of stability and the level of our insight into it. Disturbances and stability are multidimensional. Our understanding of them is not. We have a remarkably poor understanding of the impacts on stability of the characteristics that define many, perhaps all, of the most important elements of global change. We provide recommendations for theoreticians, empiricists and policymakers on how to better integrate the multidimensional nature of ecological stability into their research, policies and actions.

On the dimensionality of ecological stability.

Ecological stability is touted as a complex and multifaceted concept, including components such as variability, resistance, resilience, persistence and robustness. Even though a complete appreciation of the effects of perturbations on ecosystems requires the simultaneous measurement of these multiple components of stability, most ecological research has focused on one or a few of those components analysed in isolation. Here, we present a new view of ecological stability that recognises explicitly the non-independence of components of stability. This provides an approach for simplifying the concept of stability. We illustrate the concept and approach using results from a field experiment, and show that the effective dimensionality of ecological stability is considerably lower than if the various components of stability were unrelated. However, strong perturbations can modify, and even decouple, relationships among individual components of stability. Thus, perturbations not only increase the dimensionality of stability but they can also alter the relationships among components of stability in different ways. Studies that focus on single forms of stability in isolation therefore risk underestimating significantly the potential of perturbations to destabilise ecosystems. In contrast, application of the multidimensional stability framework that we propose gives a far richer understanding of how communities respond to perturbations.

Specificity and temporal dynamics of complex bacteria--sponge symbiotic interactions.

Microbes are known to form intricate and intimate relationships with most animal and plant taxa. Microbe--host symbiotic associations are poorly explored in comparison with other species interaction networks. The current paradigm on symbiosis research stems from species-poor systems where pairwise and reciprocally specialized interactions between a single microbe and a single host that coevolve are the norm. These symbioses involving just a few species are fascinating in their own right, but more diverse and complex host-associated microbial communities are increasingly found, with new emerging questions that require new paradigms and approaches. Here we adopt an intermediate complexity approach to study the specificity, phylogenetic community structure, and temporal variability of the subset of the most abundant bacteria associated with different sponge host species with diverse eco-evolutionary characteristics. We do so by using a monthly resolved annual temporal series of host-associated and free-living bacteria. Bacteria are very abundant and diverse within marine sponges, and these symbiotic interactions are hypothesized to have a very ancient origin. We show that host-bacteria reciprocal specialization depends on the temporal scale and level of taxonomic aggregation considered. Sponge hosts with similar eco-evolutionary characteristics (e.g., volume of tissue corresponding to microbes, water filtering rates, and microbial transmission type) have similar bacterial phylogenetic community structure when looking at interactions aggregated over time. In general, sponge hosts hypothesized to form more intricate relationships with bacteria show a remarkably persistent bacterial community over time. Other hosts, however, show a large turnover similar to that observed for free-living bacterioplankton. Our study highlights the importance of exploring temporal variability in host--microbe interaction networks if we aim to determine how specific and persistent these poorly explored but extremely common interactions are.

Land use drives detritivore size structure and decomposition through shifts in resource quality and quantity.

Land use change and nutrient pollution are two pervasive stressors that can modify carbon cycling, as they influence the inputs and the transformation of detritus. Understanding their impact on stream food webs and on diversity is particularly pressing, as streams are largely fuelled by detrital material received from the adjacent riparian environment. Here we assess how a switch from native deciduous forest to Eucalyptus plantations and nutrient enrichment alter the size distribution of stream detritivore communities and decomposition rates of detritus. As expected, more detritus resulted in higher size-independent, or overall, abundance (i.e. higher intercept of size spectra). This change in overall abundance was mainly driven by a change of the relative contribution of large taxa (Amphipoda and Trichoptera), which changed from an average relative abundance of 55.5 to 77.2 % between the sites compared for resource quantity differences in our study. In contrast, detritus quality modified the relative abundance of large vs small individuals (i.e. size spectra slopes), with shallow slopes of size spectra (proportionately more large individuals) associated with sites with nutrient-richer waters and steeper slopes (proportionately fewer large individuals) associated with sites draining Eucalyptus plantations. Decomposition rates of alder leaves due to macroinvertebrates increased from 0.0003 to 0.0142 when relative contribution of large organisms increased (modelled slopes of size spectra: -1.00 and - 0.33, respectively), highlighting the importance of large sized individuals for ecosystem functioning. Our study reveals that land use change and nutrient pollution can greatly impair the transfer of energy through the detrital or 'brown' food web by means of intra- and inter-specific responses to quality and quantity of the detritus. These responses enable linking land use change and nutrient pollution to ecosystem productivity and carbon cycling.

Thermal mismatches explain consumer-resource dynamics in response to environmental warming.

Changing temperatures will impact food webs in ways we yet to fully understand. The thermal sensitivities of various physiological and ecological processes differ across organisms and study systems, hindering the generation of accurate predictions. One step towards improving this picture is to acquire a mechanistic understanding of how temperature change impacts trophic interactions before we can scale these insights up to food webs and ecosystems. Here, we implement a mechanistic approach centered on the thermal sensitivity of energetic balances in pairwise consumer-resource interactions, measuring the thermal dependence of energetic gain and loss for two resource and one consumer freshwater species. Quantifying the balance between energy gain and loss, we determined the temperature ranges where the balance decreased for each species in isolation (intraspecific thermal mismatch) and where a mismatch in the balance between consumer and resource species emerged (interspecific thermal mismatch). The latter reveals the temperatures for which consumer and resource energetic balances respond either differently or in the same way, which in turn informs us of the strength of top-down control. We found that warming improved the energetic balance for both resources, but reduces it for the consumer, due to the stronger thermal sensitivity of respiration compared to ingestion. The interspecific thermal mismatch yielded different patterns between the two consumer-resource pairs. In one case, the consumer-resource energetic balance became weaker throughout the temperature gradient, and in the other case it produced a U-shaped response. By also measuring interaction strength for these interaction pairs, we demonstrated the correspondence of interspecific thermal mismatches and interaction strength. Our approach accounts for the energetic traits of both consumer and resource species, which combined produce a good indication of the thermal sensitivity of interaction strength. Thus, this novel approach links thermal ecology with parameters typically explored in food-web studies.