Untangling the complex food webs of tropical rainforest streams.

Food webs depict the tangled web of trophic interactions associated with the functioning of an ecosystem. Understanding the mechanisms providing stability to these food webs is therefore vital for conservation efforts and the management of natural systems. Here, we first characterised a tropical stream meta-food web and five individual food webs using a Bayesian Hierarchical approach unifying three sources of information (gut content analysis, literature compilation and stable isotope data). With data on population-level biomass and individually measured body mass, we applied a bioenergetic model and assessed food web stability using a Lotka-Volterra system of equations. We then assessed the resilience of the system to individual species extinctions using simulations and investigated the network patterns associated with systems with higher stability. The model resulted in a stable meta-food web with 307 links among the 61 components. At the regional scale, 70% of the total energy flow occurred through a set of 10 taxa with large variation in body masses. The remaining 30% of total energy flow relied on 48 different taxa, supporting a significant dependency on a diverse community. The meta-food web was stable against individual species extinctions, with a higher resilience in food webs harbouring omnivorous fish species able to connect multiple food web compartments via weak, non-specialised interactions. Moreover, these fish species contributed largely to the spatial variation among individual food webs, suggesting that these species could operate as mobile predators connecting different streams and stabilising variability at the regional scale. Our results outline two key mechanisms of food web stability operating in tropical streams: (i) the diversity of species and body masses buffering against random and size-dependent disturbances and (ii) high regional diversity and weak omnivorous interactions of predators buffering against local stochastic variation in species composition. These mechanisms rely on high local and regional biodiversity in tropical streams, which is known to be strongly affected by human impacts. Therefore, an urgent challenge is to understand how the ongoing systematic loss of diversity jeopardises the stability of stream food webs in human-impacted landscapes.

As teias alimentares representam um emaranhado de interações tróficas associadas ao funcionamento de um ecossistema. Compreender os mecanismos que proporcionam estabilidade a estas teias alimentares é, portanto, vital para os esforços de conservação e gestão dos sistemas naturais. Aqui, primeiro caracterizamos uma meta teia alimentar de riachos tropicais e cinco teias alimentares individuais usando uma abordagem hierárquica Bayesiana unificando três fontes de informação (análise de conteúdo estomacal, compilação de literatura, dados de isótopos estáveis). Com dados sobre biomassa em nível populacional e massa corporal medida individualmente, aplicamos um modelo bioenergético e avaliamos a estabilidade da cadeia alimentar usando um sistema de equações Lotka­Volterra. Em seguida, avaliamos a resiliência do sistema às extinções de espécies individuais usando simulações e investigamos os padrões de rede associados a sistemas com maior estabilidade. O modelo resultou em uma meta teia alimentar estável com 307 ligações entre os 61 componentes. Na escala regional, 70% do fluxo total de energia ocorreu através de um conjunto de dez taxa com grande variação nas massas corporais. Os restantes 30% do fluxo total de energia dependiam de 47 taxa diferentes, apoiando uma dependência significativa de uma comunidade diversificada. A meta teia alimentar foi estável contra extinções de espécies individuais, com uma maior resiliência em teias alimentares que abrigam espécies de peixes onívoros capazes de conectar múltiplos compartimentos da teia alimentar através de interações fracas e não especializadas. Além disso, estas espécies de peixes contribuíram amplamente para a variação espacial entre as cadeias alimentares individuais, sugerindo que estas espécies poderiam operar como predadores móveis conectando diferentes riachos e estabilizando a variabilidade à escala regional. Nossos resultados descrevem dois mecanismos principais de estabilidade da cadeia alimentar operando em riachos tropicais: (i) a diversidade de espécies e massas corporais que protegem contra distúrbios aleatórios e dependentes do tamanho (ii) alta diversidade regional e fracas interações onívoras de predadores que protegem contra a variação estocástica local na composição de espécies. Estes mecanismos dependem de uma elevada biodiversidade local e regional em riachos tropicais, que são conhecidos por serem fortemente afetados pelos impactos humanos. Portanto, um desafio urgente é compreender como a contínua perda sistemática de diversidade põe em risco a estabilidade das teias alimentares em paisagens impactadas pelo homem.

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.

Land-use intensification systematically alters the size structure of aquatic communities in the Neotropics.

Land-use and land-cover transitions can affect biodiversity and ecosystem functioning in a myriad of ways, including how energy is transferred within food-webs. Size spectra (i.e. relationships between body size and biomass or abundance) provide a means to assess how food-webs respond to environmental stressors by depicting how energy is transferred from small to larger organisms. Here, we investigated changes in the size spectrum of aquatic macroinvertebrates along a broad land-use intensification gradient (from Atlantic Forest to mechanized agriculture) in 30 Brazilian streams. We expected to find a steeper size spectrum slope and lower total biomass in more disturbed streams due to higher energetic expenditure in physiologically stressful conditions, which has a disproportionate impact on large individuals. As expected, we found that more disturbed streams had fewer small organisms than pristine forest streams, but, surprisingly, they had shallower size spectrum slopes, which indicates that energy might be transferred more efficiently in disturbed streams. Disturbed streams were also less taxonomically diverse, suggesting that the potentially higher energy transfer in these webs might be channelled via a few efficient trophic links. However, because total biomass was higher in pristine streams, these sites still supported a greater number of larger organisms and longer food chains (i.e. larger size range). Our results indicate that land-use intensification decreases ecosystem stability and enhances vulnerability to population extinctions by reducing the possible energetic pathways while enhancing efficiency between the remaining food-web linkages. Our study represents a step forward in understanding how land-use intensification affects trophic interactions and ecosystem functioning in aquatic systems.

Human pressure drives biodiversity-multifunctionality relationships in large Neotropical wetlands.

Many studies have shown that biodiversity regulates multiple ecological functions that are needed to maintain the productivity of a variety of ecosystem types. What is unknown is how human activities may alter the 'multifunctionality' of ecosystems through both direct impacts on ecosystems and indirect effects mediated by the loss of multifaceted biodiversity. Using an extensive database of 72 lakes spanning four large Neotropical wetlands in Brazil, we demonstrate that species richness and functional diversity across multiple larger (fish and macrophytes) and smaller (microcrustaceans, rotifers, protists and phytoplankton) groups of aquatic organisms are positively associated with ecosystem multifunctionality. Whereas the positive association between smaller organisms and multifunctionality broke down with increasing human pressure, this positive relationship was maintained for larger organisms despite the increase in human pressure. Human pressure impacted multifunctionality both directly and indirectly through reducing species richness and functional diversity of multiple organismal groups. These findings provide further empirical evidence about the importance of aquatic biodiversity for maintaining wetland multifunctionality. Despite the key role of biodiversity, human pressure reduces the diversity of multiple groups of aquatic organisms, eroding their positive impacts on a suite of ecological functions that sustain wetlands.

Consistent predator-prey biomass scaling in complex food webs.

The ratio of predator-to-prey biomass is a key element of trophic structure that is typically investigated from a food chain perspective, ignoring channels of energy transfer (e.g. omnivory) that may govern community structure. Here, we address this shortcoming by characterising the biomass structure of 141 freshwater, marine and terrestrial food webs, spanning a broad gradient in community biomass. We test whether sub-linear scaling between predator and prey biomass (a potential signal of density-dependent processes) emerges within ecosystem types and across levels of biological organisation. We find a consistent, sub-linear scaling pattern whereby predator biomass scales with the total biomass of their prey with a near ¾-power exponent within food webs - i.e. more prey biomass supports proportionally less predator biomass. Across food webs, a similar sub-linear scaling pattern emerges between total predator biomass and the combined biomass of all prey within a food web. These general patterns in trophic structure are compatible with a systematic form of density dependence that holds among complex feeding interactions across levels of organization, irrespective of ecosystem type.

Systematic variation in food web body-size structure linked to external subsidies.

The relationship between body mass (M) and size class abundance (N) depicts patterns of community structure and energy flow through food webs. While the general assumption is that M and N scale linearly (on log-log axes), nonlinearity is regularly observed in natural systems, and is theorized to be driven by nonlinear scaling of trophic level (TL) with M resulting in the rapid transfer of energy to consumers in certain size classes. We tested this hypothesis with data from 31 stream food webs. We predicted that allochthonous subsidies higher in the web results in nonlinear M-TL relationships and systematic abundance peaks in macroinvertebrate and fish size classes (latter containing salmonids), that exploit terrestrial plant material and terrestrial invertebrates, respectively. Indeed, both M-N and M-TL significantly deviated from linear relationships and the observed curvature in M-TL scaling was inversely related to that observed in M-N relationships. Systemic peaks in M-N, and troughs in M-TL occurred in size classes dominated by generalist invertebrates, and brown trout. Our study reveals how allochthonous resources entering high in the web systematically shape community size structure and demonstrates the relevance of a generalized metabolic scaling model for understanding patterns of energy transfer in energetically 'open' food webs.

A Metabolic Perspective of Stochastic Community Assembly.

Metabolism controls the pace of life, driving major ecological patterns. We propose that the scaling of metabolism with temperature influences neutral processes of community assembly by controlling population dynamics independently of species identities. This perspective provides new insights into the prevalence of niche and neutral processes through universal energetic constraints.

The riverine bioreactor: An integrative perspective on biological decomposition of organic matter across riverine habitats.

Riverine ecosystems can be conceptualized as 'bioreactors' (the riverine bioreactor) which retain and decompose a wide range of organic substrates. The metabolic performance of the riverine bioreactor is linked to their community structure, the efficiency of energy transfer along food chains, and complex interactions among biotic and abiotic environmental factors. However, our understanding of the mechanistic functioning and capacity of the riverine bioreactor remains limited. We review the state of knowledge and outline major gaps in the understanding of biotic drivers of organic matter decomposition processes that occur in riverine ecosystems, across habitats, temporal dimensions, and latitudes influenced by climate change. We propose a novel, integrative analytical perspective to assess and predict decomposition processes in riverine ecosystems. We then use this model to analyse data to demonstrate that the size-spectra of a community can be used to predict decomposition rates by analysing an illustrative dataset. This modelling methodology allows comparison of the riverine bioreactor's performance across habitats and at a global scale. Our integrative analytical approach can be applied to advance understanding of the functioning and efficiency of the riverine bioreactor as hotspots of metabolic activity. Application of insights gained from such analyses could inform the development of strategies that promote the functioning of the riverine bioreactor across global ecosystems.

Depth and vertical hydrodynamics constrain the size structure of a lowland streambed community.

Abundance-body mass (N-M) relationships are prominent macroecological patterns and provide an integrated measurement of the structure and energy flow through natural communities. However, little is known about how N-M relationships are constrained by local environmental conditions. Here, we quantify how sediment depth and direction of surface-groundwater exchange (vertical hydrodynamics), two major drivers of the streambed ecology, determine N-M scaling in a sandy lowland European stream. Streambed assemblages included flagellates, ciliates, meiofauna and macroinvertebrates, and spanned five orders of magnitude in body mass. We detected a significant interaction of body mass with depth and vertical hydrodynamics with a sharp reduction in N-M slopes in the hyporheic zone and under upwelling conditions. These results revealed that streambed assemblages become more size-structured as environmental constraints increase with direct implications for the metabolic capacity and functioning of the system.

Comparing biotic drivers of litter breakdown across stream compartments.

Litter breakdown in the streambed is an important pathway in organic carbon cycling and energy transfer in the biosphere that is mediated by a wide range of streambed organisms. However, most research on litter breakdown to date has focused on a small fraction of the taxa that drive it (e.g. microbial vs. macroinvertebrate-mediated breakdown) and has been limited to the benthic zone (BZ). Despite the importance of the hyporheic zone (HZ) as a bioreactor, little is known about what, or who, mediates litter breakdown in this compartment and whether breakdown rates differ between the BZ and HZ. Here, we explore the relationship between litter breakdown and the variation in community structure of benthic and hyporheic communities by deploying two standardized bioassays (cotton strips and two types of commercially available tea bags) in 30 UK streams that encompass a range of environmental conditions. Then, we modelled these assays as a response of the streambed compartment and the biological features of the streambed assemblage (Prokaryota, Protozoa and Eumetazoa invertebrates) to understand the generality and efficiency of litter processing across communities. Litter breakdown was much faster in the BZ compared with the HZ (around 5 times higher for cotton strips and 1.5 times faster for the tea leaves). However, differences in litter breakdown between the BZ and the HZ were mediated by the biological features of the benthos and the hyporheos. Biomass of all the studied biotic groups, α-diversity of Eumetazoa invertebrates and metabolic diversity of Prokaryota were important predictors that were positively related to breakdown coefficients demonstrating their importance in the functioning of the streambed ecosystem. Our study uses a novel multimetric bioassay that is able to disentangle the contribution by Prokaryota, Protozoa and Eumetazoa invertebrates to litter breakdown. In doing so, our study reveals new insights into how organic matter decomposition is partitioned across biota and streambed compartments.

Energetic equivalence underpins the size structure of tree and phytoplankton communities.

The size structure of autotroph communities - the relative abundance of small vs. large individuals - shapes the functioning of ecosystems. Whether common mechanisms underpin the size structure of unicellular and multicellular autotrophs is, however, unknown. Using a global data compilation, we show that individual body masses in tree and phytoplankton communities follow power-law distributions and that the average exponents of these individual size distributions (ISD) differ. Phytoplankton communities are characterized by an average ISD exponent consistent with three-quarter-power scaling of metabolism with body mass and equivalence in energy use among mass classes. Tree communities deviate from this pattern in a manner consistent with equivalence in energy use among diameter size classes. Our findings suggest that whilst universal metabolic constraints ultimately underlie the emergent size structure of autotroph communities, divergent aspects of body size (volumetric vs. linear dimensions) shape the ecological outcome of metabolic scaling in forest vs. pelagic ecosystems.

Bending the rules: exploitation of allochthonous resources by a top-predator modifies size-abundance scaling in stream food webs.

Body mass-abundance (M-N) allometries provide a key measure of community structure, and deviations from scaling predictions could reveal how cross-ecosystem subsidies alter food webs. For 31 streams across the UK, we tested the hypothesis that linear log-log M-N scaling is shallower than that predicted by allometric scaling theory when top predators have access to allochthonous prey. These streams all contained a common and widespread top predator (brown trout) that regularly feeds on terrestrial prey and, as hypothesised, deviations from predicted scaling increased with its dominance of the fish assemblage. Our study identifies a key beneficiary of cross-ecosystem subsidies at the top of stream food webs and elucidates how these inputs can reshape the size-structure of these 'open' systems.

Higher biodiversity is required to sustain multiple ecosystem processes across temperature regimes.

Biodiversity loss is occurring rapidly worldwide, yet it is uncertain whether few or many species are required to sustain ecosystem functioning in the face of environmental change. The importance of biodiversity might be enhanced when multiple ecosystem processes (termed multifunctionality) and environmental contexts are considered, yet no studies have quantified this explicitly to date. We measured five key processes and their combined multifunctionality at three temperatures (5, 10 and 15 °C) in freshwater aquaria containing different animal assemblages (1-4 benthic macroinvertebrate species). For single processes, biodiversity effects were weak and were best predicted by additive-based models, i.e. polyculture performances represented the sum of their monoculture parts. There were, however, significant effects of biodiversity on multifunctionality at the low and the high (but not the intermediate) temperature. Variation in the contribution of species to processes across temperatures meant that greater biodiversity was required to sustain multifunctionality across different temperatures than was the case for single processes. This suggests that previous studies might have underestimated the importance of biodiversity in sustaining ecosystem functioning in a changing environment.

Warming alters community size structure and ecosystem functioning.

Global warming can affect all levels of biological complexity, though we currently understand least about its potential impact on communities and ecosystems. At the ecosystem level, warming has the capacity to alter the structure of communities and the rates of key ecosystem processes they mediate. Here we assessed the effects of a 4°C rise in temperature on the size structure and taxonomic composition of benthic communities in aquatic mesocosms, and the rates of detrital decomposition they mediated. Warming had no effect on biodiversity, but altered community size structure in two ways. In spring, warmer systems exhibited steeper size spectra driven by declines in total community biomass and the proportion of large organisms. By contrast, in autumn, warmer systems had shallower size spectra driven by elevated total community biomass and a greater proportion of large organisms. Community-level shifts were mirrored by changes in decomposition rates. Temperature-corrected microbial and macrofaunal decomposition rates reflected the shifts in community structure and were strongly correlated with biomass across mesocosms. Our study demonstrates that the 4°C rise in temperature expected by the end of the century has the potential to alter the structure and functioning of aquatic ecosystems profoundly, as well as the intimate linkages between these levels of ecological organization.

Testing effects of consumer richness, evenness and body size on ecosystem functioning.

1. Numerous studies have revealed (usually positive) relationships between biodiversity and ecosystem functioning (B-EF), but the underpinning drivers are rarely addressed explicitly, hindering the development of a more predictive understanding. 2. We developed a suite of statistical models (where we combined existing models with novel ones) to test for richness and evenness effects on detrital processing in freshwater microcosms. Instead of using consumer species as biodiversity units, we used two size classes within three species (six types). This allowed us to test for diversity effects and also to focus on the role of body size and biomass. 3. Our statistical models tested for (i) whether performance in polyculture was more than the sum of its parts (non-additive effects), (ii) the effects of specific type combinations (assemblage identity effects) and (iii) whether types behaved differently when their absolute or relative abundances were altered (e.g. because type abundance in polyculture was lower compared with monoculture). The latter point meant we did not need additional density treatments. 4. Process rates were independent of richness and evenness and all types performed in an additive fashion. The performance of a type was mainly driven by the consumers' metabolic requirements (connected to body size). On an assemblage level, biomass explained a large proportion of detrital processing rates. 5. We conclude that B-EF studies would benefit from widening their statistical approaches. Further, they need to consider biomass of species assemblages and whether biomass is comprised of small or large individuals, because even if all species are present in the same biomass, small species (or individuals) will perform better.

Climate change and freshwater ecosystems: impacts across multiple levels of organization.

Fresh waters are particularly vulnerable to climate change because (i) many species within these fragmented habitats have limited abilities to disperse as the environment changes; (ii) water temperature and availability are climate-dependent; and (iii) many systems are already exposed to numerous anthropogenic stressors. Most climate change studies to date have focused on individuals or species populations, rather than the higher levels of organization (i.e. communities, food webs, ecosystems). We propose that an understanding of the connections between these different levels, which are all ultimately based on individuals, can help to develop a more coherent theoretical framework based on metabolic scaling, foraging theory and ecological stoichiometry, to predict the ecological consequences of climate change. For instance, individual basal metabolic rate scales with body size (which also constrains food web structure and dynamics) and temperature (which determines many ecosystem processes and key aspects of foraging behaviour). In addition, increasing atmospheric CO(2) is predicted to alter molar CNP ratios of detrital inputs, which could lead to profound shifts in the stoichiometry of elemental fluxes between consumers and resources at the base of the food web. The different components of climate change (e.g. temperature, hydrology and atmospheric composition) not only affect multiple levels of biological organization, but they may also interact with the many other stressors to which fresh waters are exposed, and future research needs to address these potentially important synergies.