Host phylogeny shapes viral transmission networks in an island ecosystem.

Virus transmission between host species underpins disease emergence. Both host phylogenetic relatedness and aspects of their ecology, such as species interactions and predator-prey relationships, may govern rates and patterns of cross-species virus transmission and hence zoonotic risk. To address the impact of host phylogeny and ecology on virus diversity and evolution, we characterized the virome structure of a relatively isolated island ecological community in Fiordland, New Zealand, that are linked through a food web. We show that phylogenetic barriers that inhibited cross-species virus transmission occurred at the level of host phyla (between the Chordata, Arthropoda and Streptophyta) as well as at lower taxonomic levels. By contrast, host ecology, manifest as predator-prey interactions and diet, had a smaller influence on virome composition, especially at higher taxonomic levels. The virus-host community comprised a 'small world' network, in which hosts with a high diversity of viruses were more likely to acquire new viruses, and generalist viruses that infect multiple hosts were more likely to infect additional species compared to host specialist viruses. Such a highly connected ecological community increases the likelihood of cross-species virus transmission, particularly among closely related species, and suggests that host generalist viruses present the greatest risk of disease emergence.

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.

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.

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.

Ecological network complexity scales with area.

Larger geographical areas contain more species-an observation raised to a law in ecology. Less explored is whether biodiversity changes are accompanied by a modification of interaction networks. We use data from 32 spatial interaction networks from different ecosystems to analyse how network structure changes with area. We find that basic community structure descriptors (number of species, links and links per species) increase with area following a power law. Yet, the distribution of links per species varies little with area, indicating that the fundamental organization of interactions within networks is conserved. Our null model analyses suggest that the spatial scaling of network structure is determined by factors beyond species richness and the number of links. We demonstrate that biodiversity-area relationships can be extended from species counts to higher levels of network complexity. Therefore, the consequences of anthropogenic habitat destruction may extend from species loss to wider simplification of natural communities.

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.

Stoichiometric constraints modulate temperature and nutrient effects on biomass distribution and community stability.

Temperature and nutrients are two of the most important drivers of global change. Both can modify the elemental composition (i.e. stoichiometry) of primary producers and consumers. Yet their combined effect on the stoichiometry, dynamics and stability of ecological communities remains largely unexplored. To fill this gap, we extended the Rosenzweig-MacArthur consumer-resource model by including thermal dependencies, nutrient dynamics and stoichiometric constraints on both the primary producer and the consumer. We found that stoichiometric and nutrient conservation constraints dampen the paradox of enrichment and increased persistence at high nutrient levels. Nevertheless, stoichiometric constraints also reduced consumer persistence at extreme temperatures. Finally, we also found that stoichiometric constraints and nutrient dynamics can strongly influence biomass distribution across trophic levels by modulating consumer assimilation efficiency and resource growth rates along the environmental gradients. In the Rosenzweig-MacArthur model, consumer biomass exceeded resource biomass for most parameter values whereas, in the stoichiometric model, consumer biomass was strongly reduced and sometimes lower than resource biomass. Our findings highlight the importance of accounting for stoichiometric constraints as they can mediate the temperature and nutrient impact on the dynamics and functioning of ecological communities.

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.

Biodiversity as insurance: from concept to measurement and application.

Biological insurance theory predicts that, in a variable environment, aggregate ecosystem properties will vary less in more diverse communities because declines in the performance or abundance of some species or phenotypes will be offset, at least partly, by smoother declines or increases in others. During the past two decades, ecology has accumulated strong evidence for the stabilising effect of biodiversity on ecosystem functioning. As biological insurance is reaching the stage of a mature theory, it is critical to revisit and clarify its conceptual foundations to guide future developments, applications and measurements. In this review, we first clarify the connections between the insurance and portfolio concepts that have been used in ecology and the economic concepts that inspired them. Doing so points to gaps and mismatches between ecology and economics that could be filled profitably by new theoretical developments and new management applications. Second, we discuss some fundamental issues in biological insurance theory that have remained unnoticed so far and that emerge from some of its recent applications. In particular, we draw a clear distinction between the two effects embedded in biological insurance theory, i.e. the effects of biodiversity on the mean and variability of ecosystem properties. This distinction allows explicit consideration of trade-offs between the mean and stability of ecosystem processes and services. We also review applications of biological insurance theory in ecosystem management. Finally, we provide a synthetic conceptual framework that unifies the various approaches across disciplines, and we suggest new ways in which biological insurance theory could be extended to address new issues in ecology and ecosystem management. Exciting future challenges include linking the effects of biodiversity on ecosystem functioning and stability, incorporating multiple functions and feedbacks, developing new approaches to partition biodiversity effects across scales, extending biological insurance theory to complex interaction networks, and developing new applications to biodiversity and ecosystem management.

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.

Eco-evolutionary consequences of habitat warming and fragmentation in communities.

Eco-evolutionary dynamics can mediate species and community responses to habitat warming and fragmentation, two of the largest threats to biodiversity and ecosystems. The eco-evolutionary consequences of warming and fragmentation are typically studied independently, hindering our understanding of their simultaneous impacts. Here, we provide a new perspective rooted in trade-offs among traits for understanding their eco-evolutionary consequences. On the one hand, temperature influences traits related to metabolism, such as resource acquisition and activity levels. Such traits are also likely to have trade-offs with other energetically costly traits, like antipredator defences or dispersal. On the other hand, fragmentation can influence a variety of traits (e.g. dispersal) through its effects on the spatial environment experienced by individuals, as well as properties of populations, such as genetic structure. The combined effects of warming and fragmentation on communities should thus reflect their collective impact on traits of individuals and populations, as well as trade-offs at multiple trophic levels, leading to unexpected dynamics when effects are not additive and when evolutionary responses modulate them. Here, we provide a road map to navigate this complexity. First, we review single-species responses to warming and fragmentation. Second, we focus on consumer-resource interactions, considering how eco-evolutionary dynamics can arise in response to warming, fragmentation, and their interaction. Third, we illustrate our perspective with several example scenarios in which trait trade-offs could result in significant eco-evolutionary dynamics. Specifically, we consider the possible eco-evolutionary consequences of (i) evolution in thermal performance of a species involved in a consumer-resource interaction, (ii) ecological or evolutionary changes to encounter and attack rates of consumers, and (iii) changes to top consumer body size in tri-trophic food chains. In these scenarios, we present a number of novel, sometimes counter-intuitive, potential outcomes. Some of these expectations contrast with those solely based on ecological dynamics, for example, evolutionary responses in unexpected directions for resource species or unanticipated population declines in top consumers. Finally, we identify several unanswered questions about the conditions most likely to yield strong eco-evolutionary dynamics, how better to incorporate the role of trade-offs among traits, and the role of eco-evolutionary dynamics in governing responses to warming in fragmented communities.

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.

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.

Temperature variability alters the stability and thresholds for collapse of interacting species.

Temperature variability and extremes can have profound impacts on populations and ecological communities. Predicting impacts of thermal variability poses a challenge, because it has both direct physiological effects and indirect effects through species interactions. In addition, differences in thermal performance between predators and prey and nonlinear averaging of temperature-dependent performance can result in complex and counterintuitive population dynamics in response to climate change. Yet the combined consequences of these effects remain underexplored. Here, modelling temperature-dependent predator-prey dynamics, we study how changes in temperature variability affect population size, collapse and stable coexistence of both predator and prey, relative to under constant environments or warming alone. We find that the effects of temperature variation on interacting species can lead to a diversity of outcomes, from predator collapse to stable coexistence, depending on interaction strengths and differences in species' thermal performance. Temperature variability also alters predictions about population collapse-in some cases allowing predators to persist for longer than predicted when considering warming alone, and in others accelerating collapse. To inform management responses that are robust to future climates with increasing temperature variability and extremes, we need to incorporate the consequences of temperature variation in complex ecosystems. This article is part of the theme issue 'Integrative research perspectives on marine conservation'.

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.