Spatial insurance in multi‐trophic metacommunities

Metacommunity theory suggests that dispersal is a key driver of diversity and ecosystem functioning in changing environments. The capacity of dispersal to mitigate effects of environmental change might vary among trophic groups, potentially resulting in changes in trophic interactions and food web structure. In a mesocosm experiment, we compared the compositional response of bacteria, phyto‐ and zooplankton to a factorial manipulation of acidification and dispersal. We found that the buffering capacity of dispersal varied among trophic groups: dispersal alleviated the negative effect of acidification on phytoplankton diversity mid‐experiment, but had no effect on the diversity of zooplankton and bacteria. Likewise, trophic groups differed in whether dispersal facilitated compositional change. Dispersal accelerated changes in phytoplankton composition under acidification, possibly mediated by changes in trophic interactions, but had no effect on the composition of zooplankton and bacteria. Overall, our results suggest that the potential for spatial insurance can vary among trophic groups.     

Planktonic dispersal dampens temporal trophic cascades in pond metacommunities

Trophic cascades, in which changes in predation affect the biomass of lower trophic levels, vary substantially in strength and incidence. Most work to explain this variation has focused on local factors and has ignored larger regional effects. To study how metacommunity dynamics can alter trophic cascades, we constructed mesocosm metacommunities consisting of three pond communities with heterogeneous levels of fish predation and examined how planktonic dispersal rate (5–140% per week) affected biomass partitioning. Two of the three communities differed continually in the occurrence of fish and supported different but constant environments in a 'spatial trophic cascade,' while the third community supported temporally variable fish occurrence in a 'temporal trophic cascade.' We find that the presence, but the not the magnitude, of dispersal dampens temporal trophic cascades through an increase in grazer biomass. In contrast, dispersal has no effect on the strength of spatial cascades due to strong sorting pressures in the communities with constant presence or absence of fish as top predators.     

Weak trophic interactions and the balance of enriched metacommunities

Weak trophic interactions have been shown to promote the stability of ecological food webs characterized by perfect mixing. However, their importance at the landscape level and response to enrichment has not been extensively examined. In this paper we examine the food-web model explored by McCann et al. [1998. Weak trophic interactions and the balance of nature. Nature 395, 794-798]. The model is expanded into a metacommunity construct where local communities are coupled through global or local dispersal. We analyze global and local stability, as well as spatial synchrony in relation to trophic interaction strength and dispersal regimes. Results reveal that weak interactions can operate through two scale-dependent mechanisms: (i) under low local dispersal regimes, local stabilization of each community under weak interactions directly scales-up to global stability. (ii) Under high local dispersal, asynchronous local destabilization associated with weak interactions proves the driver behind global stability. In the face of enrichment, weak trophic interactions are shown to be instrumental in promoting global stability when dispersal is local. These results demonstrate how the importance of weak trophic interactions can be generalized at the landscape level despite contrary local predictions.     

Network structure and biodiversity loss in food webs: robustness increases with connectance

Food-web structure mediates dramatic effects of biodiversity loss including secondary and `cascading' extinctions. We studied these effects by simulating primary species loss in 16 food webs from terrestrial and aquatic ecosystems and measuring robustness in terms of the secondary extinctions that followed. As observed in other networks, food webs are more robust to random removal of species than to selective removal of species with the most trophic links to other species. More surprisingly, robustness increases with food-web connectance but appears independent of species richness and omnivory. In particular, food webs experience `rivet-like' thresholds past which they display extreme sensitivity to removal of highly connected species. Higher connectance delays the onset of this threshold. Removing species with few trophic connections generally has little effect though there are several striking exceptions. These findings emphasize how the number of species removed affects ecosystems differently depending on the trophic functions of species removed.     

Network isolation and local diversity in neutral metacommunities

Biologists seek an understanding of the biological and environmental factors determining local community diversity. Recent advances in metacommunity ecology, and neutral theory in particular, highlight the importance of dispersal processes interacting with the spatial structure of a landscape for generating spatial patterns and maintaining biodiversity. The relative spatial isolation of a community is traditionally thought to have a large influence on local diversity. However, isolation remains an elusive concept to quantify, particularly in metacommunities with complex spatial structure. We represent the metacommunity as a network of local communities, and use network centrality measures to quantify the isolation of a local community. Using spatially explicit neutral theory, we examine how node position predicts variation in alpha diversity across a metacommunity. We find that diversity increases with node centrality in the network, but only when centrality is measured on a given scale in the network that widens with increasing dispersal rates and narrows with increasing evolutionary rates. More generally, complex biodiversity patterns form only when the underlying geography has structure on this critical scale. This provides a framework for understanding the influence of spatial geographic structure on global biodiversity patterns.     

A heatwave increases turnover and regional dominance in microbenthic metacommunities

While the effect of the global biodiversity crisis on local species loss is still debated, there is empirical evidence for major changes in local biodiversity attributed to increased species turnover. In communities exposed to a climate stressor, species turnover can lead to increased dominance of well-adapted species and consequently to an overall decline in species diversity. Despite the known importance of species turnover for community dynamics and functioning, experimental results on the connection between biodiversity loss and species turnover are scarce. We still do not fully understand which specific factors increase the rate of change in species composition, especially when considering natural compared to artificially lab assembled communities. In the present study, we experimentally tested whether a heatwave and dispersal increased species turnover and decreased species diversity in natural benthic diatom communities with different initial species compositions. We found that on the local scale, dispersal had overall positive effects on species richness while the relationship between exposure to the heatwave, species turnover, and diversity depended on initial community composition. However, on the regional (i.e. metacommunity) scale, exposure to the heatwave and dispersal both increased turnover and decreased Shannon diversity by almost 50%. Turnover in these metacommunities was not caused by a loss of species, but rather by a change in dominance patterns leading to homogenization, and consequently decreased diversity. Our study shows that climate change can destabilize community composition and degrade species diversity, but still after ca. 15 generations does not decrease the number of species in the community, demonstrating that the response of species diversity and richness to changing conditions can be fundamentally decoupled on ecological time scales.     

Dispersal and diversity in experimental metacommunities: linking theory and practice

There has been a recent rise in the number of experiments investigating the effect of dispersal on diversity, with many of the predictions for these tests derived from metacommunity theory. Despite the promise of linking observed relationships between dispersal and diversity to underlying metacommunity processes, empirical studies have faced challenges in providing robust tests of theory. We review experimental studies that have tested how dispersal affects metacommunity diversity to determine why shortcomings emerge, and to provide a framework for empirical tests of theory that capture the processes structuring diversity in natural metacommunities. We first summarize recent experimental work to outline trends in results and to highlight common methods that cause a misalignment between empirical studies and the processes described by theory. We then identify the undesired implications of three widely used experimental methods that homogenize metacommunity structure or species traits, and present alternative methods that have been used to successfully integrate experiments and theory in a biologically relevant way. Finally, we present methodological and theoretical insights from three related ecological fields (coexistence, food web and priority effects theory) that, if integrated into metacommunity experiments, could help isolate the independent and joint effects of local interactions and dispersal on diversity, and reveal the mechanisms underlying observed dispersal–diversity patterns. Together, these methods can provide stronger tests of existing theory and stimulate new theoretical explorations. Synthesis Although metacommunity experiments offer a unique opportunity to test classic and emerging theory on the relationship between dispersal and diversity, several common challenges have hindered robust tests of theory. We outline how emerging theory on the invasion criterion, food webs and priority effects could be help clarify when and how dispersal affects metacommunity diversity, and identify when experimental approaches that homogenize metacommunities fail to test existing theory. By forging better links between theoretical and empirical work, we hope to motivate novel and improved experimental approaches to understanding the joint effects of local and regional processes on diversity.     

Species diversity in neutral metacommunities: a network approach

Biologists seek an understanding of the processes underlying spatial biodiversity patterns. Neutral theory links those patterns to dispersal, speciation and community drift. Here, we advance the spatially explicit neutral model by representing the metacommunity as a network of smaller communities. Analytic theory is presented for a set of equilibrium diversity patterns in networks of communities, facilitating the exploration of parameter space not accessible by simulation. We use this theory to evaluate how the basic properties of a metacommunity – connectivity, size, and speciation rate – determine overall metacommunity γ -diversity, and how that is partitioned into α - and β -components. We find spatial structure can increase γ -diversity relative to a well-mixed model, even when θ is held constant. The magnitude of deviations from the well-mixed model and the partitioning into α - and β -diversity is related to the ratio of migration and speciation rates. γ -diversity scales linearly with metacommunity size even as α - and β -diversity scale nonlinearly with size.     

Predators alter the scaling of diversity in prey metacommunities

Although predator effects on the number of locally coexisting species are well understood, there are few formal predictions of how these local predator effects influence patterns of prey diversity at larger spatial scales. Building on the theory of island biogeography, we develop a simple model that describes how predators can alter the scaling of diversity in prey metacommunities and compares the effects of generalist and specialist predators on regional prey diversity. Generalist predators, which consume prey randomly with respect to species identity, are predicted to reduce α‐diversity and increase β‐diversity thereby maintaining regional diversity (γ‐diversity). Alternatively, specialist predators, which filter out prey species intolerant of predators, are predicted to reduce bothα‐diversity andβ‐diversity by causing the same prey species to be extirpated in each locality, resulting in regional prey species extinctions and lower γ‐diversity. These distinct effects of generalist and specialist predators on prey diversity at different spatial scales are uniquely shaped by the extent of predation within those metacommunities. Overall, our model results make general predictions for how different types of predators can differentially affect prey diversity across spatial scales, allowing a more complete understanding of the possible implications of predator eradications or introductions for biodiversity.     

Dispersal-mediated trophic interactions can generate apparent patterns of dispersal limitation in aquatic metacommunities

Dispersal is a major organising force in metacommunities, which may facilitate compositional responses of local communities to environmental change and affect ecosystem function. Organism groups differ widely in their dispersal abilities and their communities are therefore expected to have different adaptive abilities. In mesocosms, we studied the simultaneous compositional response of three plankton communities (zoo-, phyto- and bacterioplankton) to a primary productivity gradient and evaluated how this response was mediated by dispersal intensity. Dispersal enhanced responses in all three planktonic groups, which also affected ecosystem functioning. Yet, variation partitioning analyses indicated that responses in phytoplankton and bacterial communities were not only controlled by dispersal directly but also indirectly through complex trophic interactions. Our results indicate that metacommunity patterns emerging from dispersal can cascade through the food web and generate patterns of apparent dispersal limitation in organisms at other trophic levels.     

Spatial heterogeneity of biomass turnover has contrasting effects on synchrony and stability in trophic metacommunities

Spatial heterogeneity is a fundamental feature of ecosystems, and ecologists have identified it as a factor promoting the stability of population dynamics. In particular, differences in interaction strengths and resource supply between patches generate an asymmetry of biomass turnover with a fast and a slow patch coupled by a mobile predator. Here, we demonstrate that asymmetry leads to opposite stability patterns in metacommunities receiving localized perturbations depending on the characteristics of the perturbed patch. Perturbing prey in the fast patch synchronizes the dynamics of prey biomass between the two patches and destabilizes predator dynamics by increasing the predator's temporal variability. Conversely, perturbing prey in the slow patch decreases the synchrony of the prey's dynamics and stabilizes predator dynamics. Our results have implications for conservation ecology and suggest reinforcing protection policies in fast patches to dampen the effects of perturbations and promote the stability of population dynamics at the regional scale.     

Ecological community integration increases with added trophic complexity

The existence of functional biological organization at the level of multi-species communities has long been contested in ecology and evolutionary biology. I found that adding a trophic level to simulated ecological communities enhanced their ability to compete at the community level, increasing the likelihood of one community forcing all or most species in a second community to extinction. Community-level identity emerged within systems of interacting ecological networks, while competitive ability at the community level was enhanced by intense within-community selection pressure. These results suggest a reassessment of the nature of biological organization above the level of species, indicating that the drive toward biological integration, so prominent throughout the history of life, might extend to multi-species communities.     

Competition–defense tradeoff increases the diversity of microbial plankton communities and dampens trophic cascades

The competition–defense tradeoff is a significant source of functional diversity in ecological communities. Here, we present a theoretical framework to describe the competition–defense tradeoff and apply it to a size‐based model of a unicellular plankton community. Specifically, we investigate how the emergent community structure depends on the shape of the tradeoff, and on whether the cost of defense is paid for by a lowered resource affinity or by an elevated metabolic rate. The inclusion of defense affects the size distribution and trophic strategies of the emerging community dependent on environmental conditions (eutrophic versus oligotrophic) and leads to increased diversity in size and trophic strategy under eutrophic conditions. Eutrophic conditions allow for better‐defended organisms than oligotrophic conditions. In most scenarios, competition–defense tradeoffs dampen trophic cascades in the seasonal cycle simulations, and increase the abundance of mixotrophs. We further demonstrate that it matters how the cost of defense is manifest (decreased affinity versus increased metabolic rate), and that it has a significant effect on the resulting plankton community (overall biomass, size and feeding strategy diversity), particularly when the efficiency of the defense increases in direct proportion to the investment. Our results demonstrate that the structure of the ecosystem crucially depends on details of the defense tradeoff. This finding highlights the importance of a mechanistic understanding of defense tradeoffs, e.g. obtained through experimental measurements of specific defense mechanisms.     

Oceanographic coupling across three trophic levels shapes source–sink dynamics in marine metacommunities

A central goal of metapopulation ecology is to determine which subpopulations have the greatest value to the larger metapopulation. That is, where are the ‘sources’ that are most essential to persistence? This question is especially relevant to benthic marine systems, where dispersal and recruitment are greatly affected by oceanographic processes. In a single‐species context, theoretical models typically identify ‘hotspots’ with high recruitment, especially high self‐recruitment, as having the highest value. However, the oceanographic forces affecting larval delivery of a given species may also influence the recruitment of that species’ predators, prey, and competitors.We present evidence from the Virgin Islands and Bahamas that oceanographic forces produce spatial coupling between the recruitment of planktivorous fishes, the recruitment of their predators, and the productivity of their zooplankton prey. We examined the consequences of this type of multi‐trophic coupling using a simple analytical population model and a multispecies numerical simulation model with parameter values based on the Virgin Islands system. In both analyses, strong coupling caused planktivores at the highest recruitment sites to experience higher mortality (a consequence of higher predator densities) but faster growth and higher fecundity (a consequence of higher zooplankton densities) than planktivores at low recruitment sites. As such, the relative strength of oceanographic coupling between the three trophic levels strongly determined whether a particular reef acted as a source or sink. In the simulation model, density‐dependent competition for zooplankton limited overall metapopulation biomass more severely than predation, so oceanographic coupling between planktivore larval supply and zooplankton productivity had a stronger effect on the metapopulation value of a patch. We argue that the potential for such tri‐trophic coupling should be incorporated into future metacommunity models and has considerable implications for the design and evaluation of marine reserves.     

Hydrological stability drives both local and regional diversity patterns in rock pool metacommunities

A main challenge associated with macro ecological gradients such as the latitudinal diversity gradient (LDG) is that proxies of potential underlying processes are often correlated at large scales. One way to reliably identify contributing processes is to show that they can lead to similar responses at local scales. Using a set of invertebrate communities from rock pool clusters along a latitudinal gradient in Australia, we investigated the importance of hydrological stability for explaining both local and regional diversity patterns in this habitat. Results show that, at both local and regional scales, habitat stability in terms of the frequency and length of inundations was strongly correlated to local alpha diversity in individual pools and to gamma diversity at the level of pool clusters. Additionally, partitioning beta diversity into components of nestedness and species turnover revealed that communities in unstable habitats were nested subsets of communities in more stable habitats. Overall, this study provides convincing mechanistic support for the climate stability hypothesis as a potential explanation for the LDG in this system. Results also indicate that when there is enough time for dispersal and colonization, regional processes can be relatively unimportant compared to local processes to explain large scale diversity patterns.     

Plant diversity induces shifts in the functional structure and diversity across trophic levels

Changes to primary producer diversity can cascade up to consumers and affect ecosystem processes. Although the effect of producer diversity on higher trophic groups have been studied, these studies often quantify taxonomy‐based measures of biodiversity, like species richness, which do not necessarily reflect the functioning of these communities. In this study, we assess how plant species richness affects the functional composition and diversity of higher trophic levels and discuss how this might affect ecosystem processes, such as herbivory, predation and decomposition. Based on six different consumer traits, we examined the functional composition of arthropod communities sampled in experimental plots that differed in plant species richness. The two components we focused on were functional variation in the consumer community structure (functional structure) and functional diversity, expressed as functional richness, evenness and divergence. We found a consistent positive effect of plant species richness on the functional richness of herbivores, carnivores, and omnivores, but not decomposers, and contrasting patterns for functional evenness and divergence. Increasing plant species richness shifted the omnivore community to more predatory and less mobile species, and the herbivore community to more specialized and smaller species. This was accompanied by a shift towards more species occurring in the vegetation than in the ground layer. Our study shows that plant species richness strongly affects the functional structure and diversity of aboveground arthropod communities. The observed shifts in body size (herbivores), specialization (herbivores), and feeding mode (omnivores) together with changes in the functional diversity may underlie previously observed increases in herbivory and predation in plant communities of higher diversity.     

Mountain metacommunities: climate and spatial connectivity shape ant diversity in a complex landscape

Understanding what drives biodiversity patterns across scales is a central goal of ecology. Both environmental gradients and spatial landscape structure have been found to be important factors influencing species distributions and community composition, and partly reflect the balance of underlying deterministic and stochastic community processes. In some systems, environmental gradients and spatial connectivity are intertwined in that steep environmental gradients serve as boundaries on species movements and impose environment‐derived complex spatial structure to metacommunities. Mountainous landscapes are prime examples of this, and recent theory has linked principles of geomorphology, environmental gradients, and spatial structure to make predictions for resulting community patterns. In this context, we examine variation in taxonomic and phylogenetic ant diversity patterns along a geographic transect spanning > 5000 m in elevational range in the Hengduan mountains of southern China. We found that environmental gradients dominate variation in both alpha and beta diversity in this landscape, with alpha diversity strongly declining with elevation and beta diversity driven by elevational differences. However, within an elevational band spatial connectivity predicts beta diversity better than geographic distance. Our findings deviate from theoretical predictions in several ways, notably alpha diversity is monotonically declining and within‐band beta diversity is invariant with increasing elevation. The discrepancies between theory and observation may be explained by differences in the Hengduan landscape from idealized fluvial landscapes, such as a lack of a mid‐elevation peak in connectivity, as well as evolutionary limits on the source pool of species available to populate metacommunities at different elevations. The latter is supported by variation in phylogenetic community structure with elevation. Our results demonstrate the power of conceptual, statistical, and theoretical frameworks that integrate the roles of environment and spatial structure in metacommunities, but that additional work is needed to bridge the gap between abstract theory and real systems.     

Evolution in metacommunities

A metacommunity can be defined as a set of communities that are linked by migration, and extinction and recolonization. In metacommunities, evolution can occur not only by processes that occur within communities such as drift and individual selection, but also by among-community processes, such as divergent selection owing to random differences among communities in species composition, and group and community-level selection. The effect of these among-community-level processes depends on the pattern of migration among communities. Migrating units may be individuals (migrant pool model), groups of individuals (single-species propagule pool model) or multi-species associations (multi-species propagule pool model). The most interesting case is the multi-species propagule pool model. Although this pattern of migration may a priori seem rare, it becomes more plausible in small well-defined 'communities' such as symbiotic associations between two or a few species. Theoretical models and experimental studies show that community selection is potentially an effective evolutionary force. Such evolution can occur either through genetic changes within species or through changes in the species composition of the communities. Although laboratory studies show that community selection can be important, little is known about how important it is in natural populations.     

Simultaneously estimating food web connectance and structure with uncertainty

1. Food web models explain and predict the trophic interactions in a food web, and they can infer missing interactions among the organisms. The allometric diet breadth model (ADBM) is a food web model based on the foraging theory. In the ADBM, the foraging parameters are allometrically scaled to body sizes of predators and prey. In Petchey et al. (Proceedings of the National Academy of Sciences, 2008; 105: 4191), the parameterization of the ADBM had two limitations: (a) the model parameters were point estimates and (b) food web connectance was not estimated.
2. The novelty of our current approach is: (a) We consider multiple predictions from the ADBM by parameterizing it with approximate Bayesian computation, to estimate parameter distributions and not point estimates. (b) Connectance emerges from the parameterization, by measuring model fit using the true skill statistic, which takes into account prediction of both the presences and absences of links.
3. We fit the ADBM using approximate Bayesian computation to 12 observed food webs from a wide variety of ecosystems. Estimated connectance was consistently greater than previously found. In some of the food webs, considerable variation in estimated parameter distributions occurred and resulted in considerable variation (i.e., uncertainty) in predicted food web structure.
4. These results lend weight to the possibility that the observed food web data is missing some trophic links that do actually occur. It also seems likely that the ADBM likely predicts some links that do not exist. The latter could be addressed by accounting in the ADBM for additional traits other than body size. Further work could also address the significance of uncertainty in parameter estimates for predicted food web responses to environmental change.

     

Decoupled jaws promote trophic diversity in cichlid fishes

Functional decoupling of oral and pharyngeal jaws is widely considered to have expanded the ecological repertoire of cichlid fishes. But, the degree to which the evolution of these jaw systems is decoupled and whether decoupling has impacted trophic diversification remains unknown. Focusing on the large Neotropical radiation of cichlids, we ask whether oral and pharyngeal jaw evolution is correlated and how their evolutionary rates respond to feeding ecology. In support of decoupling, we find relaxed evolutionary integration between the two jaw systems, resulting in novel trait combinations that potentially facilitate feeding mode diversification. These outcomes are made possible by escaping the mechanical trade-off between force transmission and mobility, which characterizes a single jaw system that functions in isolation. In spite of the structural independence of the two jaw systems, results using a Bayesian, state-dependent, relaxed-clock model of multivariate Brownian motion indicate strongly aligned evolutionary responses to feeding ecology. So, although decoupling of prey capture and processing functions released constraints on jaw evolution and promoted trophic diversity in cichlids, the natural diversity of consumed prey has also induced a moderate degree of evolutionary integration between the jaw systems, reminiscent of the original mechanical trade-off between force and mobility.