Dynamics of ecosystem services along ecological network seascapes

Human societies depend on services provided by ecosystems, from local needs as clean water and pest control to global services like ozone layer and the ocean biological pump. Ecosystem services are intrinsically linked to the states of the ecosystem, which are, in turn, governed by a complex web of ecological interactions. These interactions and, consequently, the services they support, are increasingly under threat from environmental changes driven by human activities. Therefore, safeguarding these vital services require an understanding of how the structure and dynamics of ecological interactions are affected by environmental change. A critical step towards this goal is the development of an integrative theoretical framework that can elucidate how ecosystem services are sustained or impaired by interactions within these complex ecosystems in fluctuating environments. Recent years have seen significant progress in quantitatively characterizing the organization and the dynamics of ecological interactions through the study of ecological networks. However, linking temporally varying network structure in fluctuating environments, the seascapes of ecological networks, and their impact on ecosystem services remains a challenge. We propose an approach based upon merging empirical ecological network analysis with Boolean functions and modeling techniques accounting for fluctuating environments to tackle how ecosystem services are affected by the changing structure and dynamics of ecological networks. The approach aims to contribute to the study of how the organization of ecological interactions affects the persistence of ecosystem services. Specifically, we discuss how this approach can be used provide new insights into how environmental change affect the relationship between ecological networks and ecosystem services. The combination of information on ecosystem services, Boolean networks and fluctuating environments might allow to enhance the research around conservation strategies for preserving biodiversity and ecosystem services in the face of ongoing environmental change.

Fifty years of capacity building in the search for new marine natural products.

The Convention on Biological Diversity, and the Nagoya Protocol in particular, provide a framework for the fair and equitable sharing of benefits arising from the utilization of biological resources and traditional knowledge, and ultimately aim to promote capacity-building in the developing world. However, measuring capacity-building is a challenging task due to its intangible nature. By compiling and analyzing a database of scientific peer-reviewed publications over a period of 50 y (1965 to 2015), we investigated capacity-building in global marine natural product discovery. We used publication and authorship metrics to assess how the capacity to become scientifically proficient, prolific, and independent has changed in bioprospecting countries. Our results show that marine bioprospecting is a dynamically growing field of research with continuously increasing numbers of participating countries, publications, and scientists. Yet despite longstanding efforts to promote equitability and scientific independence, not all countries have similarly increased their capacity to explore marine biodiversity within their national jurisdiction areas. Although developing countries show an increasing trend in the number of publications, a few developed countries still account for almost one-half of all publications in the field. Multiple lines of evidence suggest that economic capacity affects how well countries with species-rich marine ecosystems can scientifically explore those resources. Overall, the capacity-building data analyzed here provides a timely contribution to the ongoing international debate about access to and benefit-sharing of biological resources for countries exploring biodiversity within and outside their national jurisdiction areas.

Positive associations among rare species and their persistence in ecological assemblages.

According to the competitive exclusion principle, species with low competitive abilities should be excluded by more efficient competitors; yet, they generally remain as rare species. Here, we describe the positive and negative spatial association networks of 326 disparate assemblages, showing a general organization pattern that simultaneously supports the primacy of competition and the persistence of rare species. Abundant species monopolize negative associations in about 90% of the assemblages. On the other hand, rare species are mostly involved in positive associations, forming small network modules. Simulations suggest that positive interactions among rare species and microhabitat preferences are the most probable mechanisms underpinning this pattern and rare species persistence. The consistent results across taxa and geography suggest a general explanation for the maintenance of biodiversity in competitive environments.

An experimental test of how parasites of predators can influence trophic cascades and ecosystem functioning.

Parasites can shape the structure and function of ecosystems by influencing both the density and traits of their hosts. Such changes in ecosystems are particularly likely when the host is a predator that mediates the dynamics of trophic cascades. Here, we experimentally tested how parasite load of a small predatory fish, the threespine stickleback, can affect the occurrence and strength of trophic cascades and ecosystem functioning. In a factorial mesocosm experiment, we manipulated the density of stickleback (low vs. high), and the level of parasite load (natural vs. reduced). In addition, we used two stickleback populations from different lineages: an eastern European lineage with a more pelagic phenotype (Lake Constance) and a western European lineage with a more benthic phenotype (Lake Geneva). We found that stickleback caused trophic cascades in the pelagic but not the benthic food chain. Evidence for pelagic trophic cascades was stronger in treatments where parasite load of stickleback was reduced with an antihelmintic medication, and where fish originated from Lake Constance (i.e., the more pelagic lineage). A structural equation model revealed that differences in stickleback lineage and parasite load were most likely to impact trophic cascades via changes in the composition, rather than overall biomass, of zooplankton communities. Overall, our results provide experimental evidence that parasites of predators can influence the cascading effects of fish on lower trophic levels with consequences on ecosystem functioning.

Detecting the macroevolutionary signal of species interactions.

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long timescales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter timescales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad-scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, although the evidence for species interactions shaping macroevolution is strong, further work using integrative and model-based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.

Size-dependent tradeoffs in seasonal freshwater environments facilitate differential salmonid migration.

BACKGROUND: Seasonal spatio-temporal variation in habitat quality and abiotic conditions leads to animals migrating between different environments around the world. Whereas mean population timing of migration is often fairly well understood, explanations for variation in migratory timing within populations are often lacking. Condition-dependent tradeoffs may be an understudied mechanism that can explain this differential migration. While fixed condition-specific thresholds have been identified in earlier work on ontogenetic niche shifts, they are rare in differential migration, suggesting that thresholds in such systems can shift based on temporally variable environmental conditions. METHODS: We introduced a model based on size-specific tradeoffs between migration and growth in seasonal environments. We focused on optimal migratory timing for first-time migrants with no knowledge of an alternative habitat, which is a crucial stage in the life history of migratory salmonids. We predicted that optimal timing would occur when individuals move from their natal habitats based on a seasonally variable ratio of predation and growth. When the ratio becomes slightly more favorable in the alternative habitat, migratory movement can occur. As it keeps shifting throughout the season, the threshold for migration is variable, allowing smaller individuals to move at later dates. We compared our model predictions to empirical data on 3 years of migratory movement of more than 800 juvenile trout of varying size from natal to feeding habitat. RESULTS: Both our model and empirical data showed that large individuals, which are assumed to have a lower predation risk in the migratory habitat, move earlier in the season than smaller individuals, whose predicted predation-to-growth ratio shifted to being favorable only later in the migratory season. Our model also predicted that the observed difference in migratory timing between large and small migrants occurred most often at low values of growth differential between the two habitats, suggesting that it was not merely high growth potential but rather the tradeoff between predation and growth that shaped differential migration patterns. CONCLUSIONS: We showed the importance of considering condition-specific tradeoffs for understanding temporal population dynamics in spatially structured landscapes. Rather than assuming a fixed threshold, which appears to be absent based on previous work on salmonids, we showed that the body-size threshold for migration changed temporally throughout the season. This allowed increasingly smaller individuals to migrate when growth conditions peaked in the migratory habitat. Our model illuminates an understudied aspect of predation as part of a condition-dependent tradeoff that shapes migratory patterns, and our empirical data back patterns predicted by this model.

Deciphering the Interdependence between Ecological and Evolutionary Networks.

Biological systems consist of elements that interact within and across hierarchical levels. For example, interactions among genes determine traits of individuals, competitive and cooperative interactions among individuals influence population dynamics, and interactions among species affect the dynamics of communities and ecosystem processes. Such systems can be represented as hierarchical networks, but can have complex dynamics when interdependencies among levels of the hierarchy occur. We propose integrating ecological and evolutionary processes in hierarchical networks to explore interdependencies in biological systems. We connect gene networks underlying predator-prey trait distributions to food webs. Our approach addresses longstanding questions about how complex traits and intraspecific trait variation affect the interdependencies among biological levels and the stability of meta-ecosystems.

Eco-evolutionary feedbacks promote fluctuating selection and long-term stability of antagonistic networks.

Studies have shown the potential for rapid adaptation in coevolving populations and that the structure of species interaction networks can modulate the vulnerability of ecological systems to perturbations. Although the feedback loop between population dynamics and coevolution of traits is crucial for understanding long-term stability in ecological assemblages, modelling eco-evolutionary dynamics in species-rich assemblages is still a challenge. We explore how eco-evolutionary feedbacks influence trait evolution and species abundances in 23 empirical antagonistic networks. We show that, if selection due to antagonistic interactions is stronger than other selective pressures, eco-evolutionary feedbacks lead to higher mean species abundances and lower temporal variation in abundances. By contrast, strong selection of antagonistic interactions leads to higher temporal variation of traits and on interaction strengths. Our results present a theoretical link between the study of the species persistence and coevolution in networks of interacting species, pointing out the ways by which coevolution may decrease the vulnerability of species within antagonistic networks to demographic fluctuation.

Comparing species interaction networks along environmental gradients.

Knowledge of species composition and their interactions, in the form of interaction networks, is required to understand processes shaping their distribution over time and space. As such, comparing ecological networks along environmental gradients represents a promising new research avenue to understand the organization of life. Variation in the position and intensity of links within networks along environmental gradients may be driven by turnover in species composition, by variation in species abundances and by abiotic influences on species interactions. While investigating changes in species composition has a long tradition, so far only a limited number of studies have examined changes in species interactions between networks, often with differing approaches. Here, we review studies investigating variation in network structures along environmental gradients, highlighting how methodological decisions about standardization can influence their conclusions. Due to their complexity, variation among ecological networks is frequently studied using properties that summarize the distribution or topology of interactions such as number of links, connectance, or modularity. These properties can either be compared directly or using a procedure of standardization. While measures of network structure can be directly related to changes along environmental gradients, standardization is frequently used to facilitate interpretation of variation in network properties by controlling for some co-variables, or via null models. Null models allow comparing the deviation of empirical networks from random expectations and are expected to provide a more mechanistic understanding of the factors shaping ecological networks when they are coupled with functional traits. As an illustration, we compare approaches to quantify the role of trait matching in driving the structure of plant-hummingbird mutualistic networks, i.e. a direct comparison, standardized by null models and hypothesis-based metaweb. Overall, our analysis warns against a comparison of studies that rely on distinct forms of standardization, as they are likely to highlight different signals. Fostering a better understanding of the analytical tools available and the signal they detect will help produce deeper insights into how and why ecological networks vary along environmental gradients.

Reintroducing Environmental Change Drivers in Biodiversity-Ecosystem Functioning Research.

For the past 20 years, research on biodiversity and ecosystem functioning (B-EF) has only implicitly considered the underlying role of environmental change. We illustrate that explicitly reintroducing environmental change drivers in B-EF research is needed to predict the functioning of ecosystems facing changes in biodiversity. Next we show how this reintroduction improves experimental control over community composition and structure, which helps to provide mechanistic insight on how multiple aspects of biodiversity relate to function and how biodiversity and function relate in food webs. We also highlight challenges for the proposed reintroduction and suggest analyses and experiments to better understand how random biodiversity changes, as studied by classic approaches in B-EF research, contribute to the shifts in function that follow environmental change.

Plate tectonics drive tropical reef biodiversity dynamics.

The Cretaceous breakup of Gondwana strongly modified the global distribution of shallow tropical seas reshaping the geographic configuration of marine basins. However, the links between tropical reef availability, plate tectonic processes and marine biodiversity distribution patterns are still unknown. Here, we show that a spatial diversification model constrained by absolute plate motions for the past 140 million years predicts the emergence and movement of diversity hotspots on tropical reefs. The spatial dynamics of tropical reefs explains marine fauna diversification in the Tethyan Ocean during the Cretaceous and early Cenozoic, and identifies an eastward movement of ancestral marine lineages towards the Indo-Australian Archipelago in the Miocene. A mechanistic model based only on habitat-driven diversification and dispersal yields realistic predictions of current biodiversity patterns for both corals and fishes. As in terrestrial systems, we demonstrate that plate tectonics played a major role in driving tropical marine shallow reef biodiversity dynamics.

Condition-dependent movement and dispersal in experimental metacommunities.

Dispersal and the underlying movement behaviour are processes of pivotal importance for understanding and predicting metapopulation and metacommunity dynamics. Generally, dispersal decisions are condition-dependent and rely on information in the broad sense, like the presence of conspecifics. However, studies on metacommunities that include interspecific interactions generally disregard condition-dependence. Therefore, it remains unclear whether and how dispersal in metacommunities is condition-dependent and whether rules derived from single-species contexts can be scaled up to (meta)communities. Using experimental protist metacommunities, we show how dispersal and movement depend on and are adjusted by the strength of interspecific interactions. We found that the predicting movement and dispersal in metacommunities requires knowledge on behavioural responses to intra- and interspecific interaction strengths. Consequently, metacommunity dynamics inferred directly from single-species metapopulations without taking interspecific interactions into account are likely flawed. Our work identifies the significance of condition-dependence for understanding metacommunity dynamics, stability and the coexistence and distribution of species.

Dispersal dynamics in food webs.

Studies of food webs suggest that limited nonrandom dispersal can play an important role in structuring food webs. It is not clear, however, whether density-dependent dispersal fits empirical patterns of food webs better than density-independent dispersal. Here, we study a spatially distributed food web, using a series of population-dispersal models that contrast density-independent and density-dependent dispersal in landscapes where sampled sites are either homogeneously or heterogeneously distributed. These models are fitted to empirical data, allowing us to infer mechanisms that are consistent with the data. Our results show that models with density-dependent dispersal fit the α, ß, and γ tritrophic richness observed in empirical data best. Our results also show that density-dependent dispersal leads to a critical distance threshold beyond which site similarity (i.e., ß tritrophic richness) starts to decrease much faster. Such a threshold can also be detected in the empirical data. In contrast, models with density-independent dispersal do not predict such a threshold. Moreover, preferential dispersal from more centrally located sites to peripheral sites does not provide a better fit to empirical data when compared with symmetric dispersal between sites. Our results suggest that nonrandom dispersal in heterogeneous landscapes is an important driver that shapes local and regional richness (i.e., α and γ tritrophic richness, respectively) as well as the distance-decay relationship (i.e., ß tritrophic richness) in food webs.

The contribution of intra- and interspecific tolerance variability to biodiversity changes along toxicity gradients.

The worldwide distribution of toxicants is an important yet understudied driver of biodiversity, and the mechanisms relating toxicity to diversity have not been adequately explored. Here, we present a community model integrating demography, dispersal and toxicant-induced effects on reproduction driven by intraspecific and interspecific variability in toxicity tolerance. We compare model predictions to 458 species abundance distributions (SADs) observed along concentration gradients of toxicants to show that the best predictions occur when intraspecific variability is five and ten times higher than interspecific variability. At high concentrations, lower settings of intraspecific variability resulted in predictions of community extinction that were not supported by the observed SADs. Subtle but significant species losses at low concentrations were predicted only when intraspecific variability dominated over interspecific variability. Our results propose intraspecific variability as a key driver for biodiversity sustenance in ecosystems challenged by environmental change.

Does sex speed up evolutionary rate and increase biodiversity?

Most empirical and theoretical studies have shown that sex increases the rate of evolution, although evidence of sex constraining genomic and epigenetic variation and slowing down evolution also exists. Faster rates with sex have been attributed to new gene combinations, removal of deleterious mutations, and adaptation to heterogeneous environments. Slower rates with sex have been attributed to removal of major genetic rearrangements, the cost of finding a mate, vulnerability to predation, and exposure to sexually transmitted diseases. Whether sex speeds or slows evolution, the connection between reproductive mode, the evolutionary rate, and species diversity remains largely unexplored. Here we present a spatially explicit model of ecological and evolutionary dynamics based on DNA sequence change to study the connection between mutation, speciation, and the resulting biodiversity in sexual and asexual populations. We show that faster speciation can decrease the abundance of newly formed species and thus decrease long-term biodiversity. In this way, sex can reduce diversity relative to asexual populations, because it leads to a higher rate of production of new species, but with lower abundances. Our results show that reproductive mode and the mechanisms underlying it can alter the link between mutation, evolutionary rate, speciation and biodiversity and we suggest that a high rate of evolution may not be required to yield high biodiversity.

Neutral biodiversity theory can explain the imbalance of phylogenetic trees but not the tempo of their diversification.

Numerous evolutionary studies have sought to explain the distribution of diversity across the limbs of the tree of life. At the same time, ecological studies have sought to explain differences in diversity and relative abundance within and among ecological communities. Traditionally, these patterns have been considered separately, but models that consider processes operating at the level of individuals, such as neutral biodiversity theory (NBT), can provide a link between them. Here, we compare evolutionary dynamics across a suite of NBT models. We show that NBT can yield phylogenetic tree topologies with imbalance closely resembling empirical observations. In general, metacommunities that exhibit greater disparity in abundance are characterized by more imbalanced phylogenetic trees. However, NBT fails to capture the tempo of diversification as represented by the distribution of branching events through time. We suggest that population-level processes might therefore help explain the asymmetry of phylogenetic trees, but that tree shape might mislead estimates of evolutionary rates unless the diversification process is modeled explicitly.

Frequency-dependent selection predicts patterns of radiations and biodiversity.

Most empirical studies support a decline in speciation rates through time, although evidence for constant speciation rates also exists. Declining rates have been explained by invoking pre-existing niches, whereas constant rates have been attributed to non-adaptive processes such as sexual selection and mutation. Trends in speciation rate and the processes underlying it remain unclear, representing a critical information gap in understanding patterns of global diversity. Here we show that the temporal trend in the speciation rate can also be explained by frequency-dependent selection. We construct a frequency-dependent and DNA sequence-based model of speciation. We compare our model to empirical diversity patterns observed for cichlid fish and Darwin's finches, two classic systems for which speciation rates and richness data exist. Negative frequency-dependent selection predicts well both the declining speciation rate found in cichlid fish and explains their species richness. For groups like the Darwin's finches, in which speciation rates are constant and diversity is lower, speciation rate is better explained by a model without frequency-dependent selection. Our analysis shows that differences in diversity may be driven by incipient species abundance with frequency-dependent selection. Our results demonstrate that genetic-distance-based speciation and frequency-dependent selection are sufficient to explain the high diversity observed in natural systems and, importantly, predict decay through time in speciation rate in the absence of pre-existing niches.

The temporal dynamics of resource use by frugivorous birds: a network approach.

Ecological network patterns are influenced by diverse processes that operate at different temporal rates. Here we analyzed whether the coupled effect of local abundance variation, seasonally phenotypic plastic responses, and species evolutionary adaptations might act in concert to shape network patterns. We studied the temporal variation in three interaction properties of bird species (number of interactions per species, interaction strength, and interaction asymmetry) in a temporal sequence of 28 plant-frugivore interaction networks spanning two years in a Mediterranean shrubland community. Three main hypotheses dealing with the temporal variation of network properties were tested, examining the effects of abundance, switching behavior between alternative food resources, and morphological traits in determining consumer interaction patterns. Our results demonstrate that temporal variation in consumer interaction patterns is explained by short-term variation in resource and bird abundances and seasonal dietary switches between alternative resources (fleshy fruits and insects). Moreover, differences in beak morphology are associated with differences in switching behavior between resources, suggesting an important role of foraging adaptations in determining network patterns. We argue that beak shape adaptations might determine generalist and specialist feeding behaviors and thus the positions of consumer species within the network. Finally, we provide a preliminary framework to interpret phylogenetic signal in plant-animal networks. Indeed, we show that the strength of the phylogenetic signal in networks depends on the relative importance of abundance, behavioral, and morphological variables. We show that these variables strongly differ in their phylogenetic signal. Consequently, we suggest that moderate and significant phylogenetic effects should be commonly observed in networks of species interactions.

Do scale-free regulatory networks allow more expression than random ones?

In this paper, we compile the network of software packages with regulatory interactions (dependences and conflicts) from Debian GNU/Linux operating system and use it as an analogy for a gene regulatory network. Using a trace-back algorithm we assemble networks from the pool of packages with both scale-free (real data) and exponential (null model) topologies. We record the maximum number of packages that can be functionally installed in the system (i.e., the active network size). We show that scale-free regulatory networks allow a larger active network size than random ones. This result might have implications for the number of expressed genes at steady state. Small genomes with scale-free regulatory topologies could allow much more expression than large genomes with exponential topologies. This may have implications for the dynamics, robustness and evolution of genomes.

Interaction strength combinations and the overfishing of a marine food web.

The stability of ecological communities largely depends on the strength of interactions between predators and their prey. Here we show that these interaction strengths are structured nonrandomly in a large Caribbean marine food web. Specifically, the cooccurrence of strong interactions on two consecutive levels of food chains occurs less frequently than expected by chance. Even when they occur, these strongly interacting chains are accompanied by strong omnivory more often than expected by chance. By using a food web model, we show that these interaction strength combinations reduce the likelihood of trophic cascades after the overfishing of top predators. However, fishing selectively removes predators that are overrepresented in strongly interacting chains. Hence, the potential for strong community-wide effects remains a threat.