The Interplay of Binary and Quantitative Structure on the Stability of Mutualistic Networks.

Understanding how the structure of biological systems impacts their resilience (broadly defined) is a recurring question across multiple levels of biological organization. In ecology, considerable effort has been devoted to understanding how the structure of interactions between species in ecological networks is linked to different broad resilience outcomes, especially local stability. Still, nearly all of that work has focused on interaction structure in presence-absence terms and has not investigated quantitative structure, i.e., the arrangement of interaction strengths in ecological networks. We investigated how the interplay between binary and quantitative structure impacts stability in mutualistic interaction networks (those in which species interactions are mutually beneficial), using community matrix approaches. We additionally examined the effects of network complexity and within-guild competition for context. In terms of structure, we focused on understanding the stability impacts of nestedness, a structure in which more-specialized species interact with smaller subsets of the same species that more-generalized species interact with. Most mutualistic networks in nature display binary nestedness, which is puzzling because both binary and quantitative nestedness are known to be destabilizing on their own. We found that quantitative network structure has important consequences for local stability. In more-complex networks, binary-nested structures were the most stable configurations, depending on the quantitative structures, but which quantitative structure was stabilizing depended on network complexity and competitive context. As complexity increases and in the absence of within-guild competition, the most stable configurations have a nested binary structure with a complementary (i.e., anti-nested) quantitative structure. In the presence of within-guild competition, however, the most stable networks are those with a nested binary structure and a nested quantitative structure. In other words, the impact of interaction overlap on community persistence is dependent on the competitive context. These results help to explain the prevalence of binary-nested structures in nature and underscore the need for future empirical work on quantitative structure.

Temporal origin of nestedness in interaction networks.

Nestedness is a common property of communication, finance, trade, and ecological networks. In networks with high levels of nestedness, the link positions of low-degree nodes (those with few links) form nested subsets of the link positions of high-degree nodes (those with many links), leading to matrix representations with characteristic upper triangular or staircase patterns. Recent theoretical work has connected nestedness to the functionality of complex systems and has suggested that it is a structural by-product of the skewed degree distributions often seen in empirical data. However, mechanisms for generating nestedness remain poorly understood, limiting the connections that can be made between system processes and observed network structures. Here, we show that a simple probabilistic model based on phenology-the timing of copresences among interaction partners-can produce nested structures and correctly predict around two-thirds of interactions in two fish market networks and around one-third of interactions in 22 plant-pollinator networks. Notably, the links most readily explained by frequent actor copresences appear to form a backbone of nested interactions, with the remaining interactions attributable to opportunistic interactions or preferences for particular interaction partners that are not routinely available.

Global determinants of insect mitochondrial genetic diversity.

Understanding global patterns of genetic diversity is essential for describing, monitoring, and preserving life on Earth. To date, efforts to map macrogenetic patterns have been restricted to vertebrates, which comprise only a small fraction of Earth's biodiversity. Here, we construct a global map of predicted insect mitochondrial genetic diversity from cytochrome c oxidase subunit 1 sequences, derived from open data. We calculate the mitochondrial genetic diversity mean and genetic diversity evenness of insect assemblages across the globe, identify their environmental correlates, and make predictions of mitochondrial genetic diversity levels in unsampled areas based on environmental data. Using a large single-locus genetic dataset of over 2 million globally distributed and georeferenced mtDNA sequences, we find that mitochondrial genetic diversity evenness follows a quadratic latitudinal gradient peaking in the subtropics. Both mitochondrial genetic diversity mean and evenness positively correlate with seasonally hot temperatures, as well as climate stability since the last glacial maximum. Our models explain 27.9% and 24.0% of the observed variation in mitochondrial genetic diversity mean and evenness in insects, respectively, making an important step towards understanding global biodiversity patterns in the most diverse animal taxon.

Metabarcoding and applied ecology with hyperdiverse organisms: Recommendations for biological control research.

Metabarcoding is revolutionizing fundamental research in ecology by enabling large-scale detection of species and producing data that are rich with community context. However, the benefits of metabarcoding have yet to be fully realized in fields of applied ecology, especially those such as classical biological control (CBC) research that involve hyperdiverse taxa. Here, we discuss some of the opportunities that metabarcoding provides CBC and solutions to the main methodological challenges that have limited the integration of metabarcoding in existing CBC workflows. We focus on insect parasitoids, which are popular and effective biological control agents (BCAs) of invasive species and agricultural pests. Accurately identifying native, invasive and BCA species is paramount, since misidentification can undermine control efforts and lead to large negative socio-economic impacts. Unfortunately, most existing publicly accessible genetic databases cannot be used to reliably identify parasitoid species, thereby limiting the accuracy of metabarcoding in CBC research. To address this issue, we argue for the establishment of authoritative genetic databases that link metabarcoding data to taxonomically identified specimens. We further suggest using multiple genetic markers to reduce primer bias and increase taxonomic resolution. We also provide suggestions for biological control-specific metabarcoding workflows intended to track the long-term effectiveness of introduced BCAs. Finally, we use the example of an invasive pest, Drosophila suzukii, in a reflective "what if" thought experiment to explore the potential power of community metabarcoding in CBC.

Analyses of three-dimensional species associations reveal departures from neutrality in a tropical forest.

The study of community spatial structure is central to understanding diversity patterns over space and species co-occurrence at local scales. Although most analytical approaches consider horizontal and vertical dimensions separately, in this study we introduce a three-dimensional spatial analysis that simultaneously includes horizontal and vertical species associations. Using tree census data (2000-2016) and allometries from the Luquillo forest plot in Puerto Rico, we show that spatial organization becomes less random over time as the forest recovered from land-use legacy effects and hurricane disturbance. Tree species vertical segregation is predominant in the forest with almost all species that co-occur in the horizontal plane avoiding each other in the vertical dimension. Horizontal segregation is less common than vertical, whereas three-dimensional aggregation (a proxy for direct tree competition) is the least frequent type of spatial association. Furthermore, dominant species are involved in more non-random spatial associations, implying that species co-occurrence is facilitated by species segregation in space. This novel three-dimensional analysis allowed us to identify and quantify tree species spatial distributions, how interspecific competition was reduced through forest structure, and how it changed over time after disturbance, in ways not detectable from two-dimensional analyses alone.

DROP: Molecular voucher database for identification of Drosophila parasitoids.

Molecular identification is increasingly used to speed up biodiversity surveys and laboratory experiments. However, many groups of organisms cannot be reliably identified using standard databases such as GenBank or BOLD due to lack of sequenced voucher specimens identified by experts. Sometimes a large number of sequences are available, but with too many errors to allow identification. Here, we address this problem for parasitoids of Drosophila by introducing a curated open-access molecular reference database, DROP (Drosophila parasitoids). Identifying Drosophila parasitoids is challenging and poses a major impediment to realize the full potential of this model system in studies ranging from molecular mechanisms to food webs, and in biological control of Drosophila suzukii. In DROP, genetic data are linked to voucher specimens and, where possible, the voucher specimens are identified by taxonomists and vetted through direct comparison with primary type material. To initiate DROP, we curated 154 laboratory strains, 856 vouchers, 554 DNA sequences, 16 genomes, 14 transcriptomes, and six proteomes drawn from a total of 183 operational taxonomic units (OTUs): 114 described Drosophila parasitoid species and 69 provisional species. We found species richness of Drosophila parasitoids to be heavily underestimated and provide an updated taxonomic catalogue for the community. DROP offers accurate molecular identification and improves cross-referencing between individual studies that we hope will catalyse research on this diverse and fascinating model system. Our effort should also serve as an example for researchers facing similar molecular identification problems in other groups of organisms.

Large herbivores transform plant-pollinator networks in an African savanna.

Pollination by animals is a key ecosystem service1,2 and interactions between plants and their pollinators are a model system for studying ecological networks,3,4 yet plant-pollinator networks are typically studied in isolation from the broader ecosystems in which they are embedded. The plants visited by pollinators also interact with other consumer guilds that eat stems, leaves, fruits, or seeds. One such guild, large mammalian herbivores, are well-known ecosystem engineers5-7 and may have substantial impacts on plant-pollinator networks. Although moderate herbivory can sometimes promote plant diversity,8 potentially benefiting pollinators, large herbivores might alternatively reduce resource availability for pollinators by consuming flowers,9 reducing plant density,10 and promoting somatic regrowth over reproduction.11 The direction and magnitude of such effects may hinge on abiotic context-in particular, rainfall, which modulates the effects of ungulates on vegetation.12 Using a long-term, large-scale experiment replicated across a rainfall gradient in central Kenya, we show that a diverse assemblage of native large herbivores, ranging from 5-kg antelopes to 4,000-kg African elephants, limited resource availability for pollinators by reducing flower abundance and diversity; this in turn resulted in fewer pollinator visits and lower pollinator diversity. Exclusion of large herbivores increased floral-resource abundance and pollinator-assemblage diversity, rendering plant-pollinator networks larger, more functionally redundant, and less vulnerable to pollinator extinction. Our results show that species extrinsic to plant-pollinator interactions can indirectly and strongly alter network structure. Forecasting the effects of environmental change on pollination services and interaction webs more broadly will require accounting for the effects of extrinsic keystone species.

Network motifs involving both competition and facilitation predict biodiversity in alpine plant communities.

Biological diversity depends on multiple, cooccurring ecological interactions. However, most studies focus on one interaction type at a time, leaving community ecologists unsure of how positive and negative associations among species combine to influence biodiversity patterns. Using surveys of plant populations in alpine communities worldwide, we explore patterns of positive and negative associations among triads of species (modules) and their relationship to local biodiversity. Three modules, each incorporating both positive and negative associations, were overrepresented, thus acting as "network motifs." Furthermore, the overrepresentation of these network motifs is positively linked to species diversity globally. A theoretical model illustrates that these network motifs, based on competition between facilitated species or facilitation between inferior competitors, increase local persistence. Our findings suggest that the interplay of competition and facilitation is crucial for maintaining biodiversity.

Isolation and characterization of diverse microbial representatives from the human skin microbiome.

BACKGROUND: The skin micro-environment varies across the body, but all sites are host to microorganisms that can impact skin health. Some of these organisms are true commensals which colonize a unique niche on the skin, while open exposure of the skin to the environment also results in the transient presence of diverse microbes with unknown influences on skin health. Culture-based studies of skin microbiota suggest that skin microbes can affect skin properties, immune responses, pathogen growth, and wound healing. RESULTS: In this work, we greatly expanded the diversity of available commensal organisms by collecting > 800 organisms from 3 body sites of 17 individuals. Our collection includes > 30 bacterial genera and 14 fungal genera, with Staphylococcus and Micrococcus as the most prevalent isolates. We characterized a subset of skin isolates for the utilization of carbon compounds found on the skin surface. We observed that members of the skin microbiota have the capacity to metabolize amino acids, steroids, lipids, and sugars, as well as compounds originating from personal care products. CONCLUSIONS: This collection is a resource that will support skin microbiome research with the potential for discovery of novel small molecules, development of novel therapeutics, and insight into the metabolic activities of the skin microbiota. We believe this unique resource will inform skin microbiome management to benefit skin health. Video abstract.

Predictor species: Improving assessments of rare species occurrence by modeling environmental co-responses.

Designing an effective conservation strategy requires understanding where rare species are located. Because rare species can be difficult to find, ecologists often identify other species called conservation surrogates that can help inform the distribution of rare species. Species distribution models typically rely on environmental data when predicting the occurrence of species, neglecting the effect of species' co-occurrences and biotic interactions. Here, we present a new approach that uses Bayesian networks to improve predictions by modeling environmental co-responses among species. For species from a European peat bog community, our approach consistently performs better than single-species models and better than conventional multi-species approaches that include the presence of nontarget species as additional independent variables in regression models. Our approach performs particularly well with rare species and when calibration data are limited. Furthermore, we identify a group of "predictor species" that are relatively common, insensitive to the presence of other species, and can be used to improve occurrence predictions of rare species. Predictor species are distinct from other categories of conservation surrogates such as umbrella or indicator species, which motivates focused data collection of predictor species to enhance conservation practices.

A systems approach reveals urban pollinator hotspots and conservation opportunities.

Urban areas are often perceived to have lower biodiversity than the wider countryside, but a few small-scale studies suggest that some urban land uses can support substantial pollinator populations. We present a large-scale, well-replicated study of floral resources and pollinators in 360 sites incorporating all major land uses in four British cities. Using a systems approach, we developed Bayesian network models integrating pollinator dispersal and resource switching to estimate city-scale effects of management interventions on plant-pollinator community robustness to species loss. We show that residential gardens and allotments (community gardens) are pollinator 'hotspots': gardens due to their extensive area, and allotments due to their high pollinator diversity and leverage on city-scale plant-pollinator community robustness. Household income was positively associated with pollinator abundance in gardens, highlighting the influence of socioeconomic factors. Our results underpin urban planning recommendations to enhance pollinator conservation, using increasing city-scale community robustness as our measure of success.

Negative biotic interactions drive predictions of distributions for species from a grassland community.

Understanding the factors that determine species' geographical distributions is important for addressing a wide range of biological questions, including where species will be able to maintain populations following environmental change. New methods for modelling species distributions include the effects of biotic interactions alongside more commonly used abiotic variables such as temperature and precipitation; however, it is not clear which types of interspecific relationship contribute to shaping species distributions and should therefore be prioritized in models. Even if some interactions are known to be influential at local spatial scales, there is no guarantee they will have similar impacts at macroecological scales. Here we apply a novel method based on information theory to determine which types of interspecific relationship drive species distributions. Our results show that negative biotic interactions such as competition have the greatest effect on model predictions for species from a California grassland community. This knowledge will help focus data collection and improve model predictions for identifying at-risk species. Furthermore, our methodological approach is applicable to any kind of species distribution model that can be specified with and without interspecific relationships.

Predicting the effect of habitat modification on networks of interacting species.

A pressing challenge for ecologists is predicting how human-driven environmental changes will affect the complex pattern of interactions among species in a community. Weighted networks are an important tool for studying changes in interspecific interactions because they record interaction frequencies in addition to presence or absence at a field site. Here we show that changes in weighted network structure following habitat modification are, in principle, predictable. Our approach combines field data with mathematical models: the models separate changes in relative species abundance from changes in interaction preferences (which describe how interaction frequencies deviate from random encounters). The models with the best predictive ability compared to data requirement are those that capture systematic changes in interaction preferences between different habitat types. Our results suggest a viable approach for predicting the consequences of rapid environmental change for the structure of complex ecological networks, even in the absence of detailed, system-specific empirical data.In a changing world, the ability to predict the impact of environmental change on ecological communities is essential. Here, the authors show that by separating species abundances from interaction preferences, they can predict the effects of habitat modification on the structure of weighted species interaction networks, even with limited data.

Linking macroecology and community ecology: refining predictions of species distributions using biotic interaction networks.

Macroecological models for predicting species distributions usually only include abiotic environmental conditions as explanatory variables, despite knowledge from community ecology that all species are linked to other species through biotic interactions. This disconnect is largely due to the different spatial scales considered by the two sub-disciplines: macroecologists study patterns at large extents and coarse resolutions, while community ecologists focus on small extents and fine resolutions. A general framework for including biotic interactions in macroecological models would help bridge this divide, as it would allow for rigorous testing of the role that biotic interactions play in determining species ranges. Here, we present an approach that combines species distribution models with Bayesian networks, which enables the direct and indirect effects of biotic interactions to be modelled as propagating conditional dependencies among species' presences. We show that including biotic interactions in distribution models for species from a California grassland community results in better range predictions across the western USA. This new approach will be important for improving estimates of species distributions and their dynamics under environmental change.

Invasion speeds in microbial systems with toxin production and quorum sensing.

The theory of invasions and invasion speeds has traditionally been studied in macroscopic systems. Surprisingly, microbial invasions have received less attention. Although microbes share many of the features associated with competition between larger-bodied organisms, they also exhibit distinctive behaviors that require new mathematical treatments to fully understand invasions in microbial systems. Most notable is the possibility for long-distance interactions, including competition between populations mediated by diffusible toxins and cooperation among individuals of a single population using quorum sensing. In this paper, we model bacterial invasion using a system of coupled partial differential equations based on Fisher's equation. Our model considers a competitive system with diffusible toxins that, in some cases, are expressed in response to quorum sensing. First, we derive analytical approximations for invasion speeds in the limits of fast and slow toxin diffusion. We then test the validity of our analytical approximations and explore intermediate rates of toxin diffusion using numerical simulations. Interestingly, we find that toxins should diffuse quickly when used offensively, but that there are two optimal strategies when toxins are used as a defense mechanism. Specifically, toxins should diffuse quickly when their killing efficacy is high, but should diffuse slowly when their killing efficacy is low. Our approach permits an explicit investigation of the properties and characteristics of diffusible compounds used in non-local competition, and is relevant for microbial systems and select macroscopic taxa, such as plants and corals, that can interact through biochemicals.

Correction: Bounds on Transient Instability for Complex Ecosystems.

[This corrects the article DOI: 10.1371/journal.pone.0157876.].

Bounds on Transient Instability for Complex Ecosystems.

Stability is a desirable property of complex ecosystems. If a community of interacting species is at a stable equilibrium point then it is able to withstand small perturbations to component species' abundances without suffering adverse effects. In ecology, the Jacobian matrix evaluated at an equilibrium point is known as the community matrix, which describes the population dynamics of interacting species. A system's asymptotic short- and long-term behaviour can be determined from eigenvalues derived from the community matrix. Here we use results from the theory of pseudospectra to describe intermediate, transient dynamics. We first recover the established result that the transition from stable to unstable dynamics includes a region of 'transient instability', where the effect of a small perturbation to species' abundances-to the population vector-is amplified before ultimately decaying. Then we show that the shift from stability to transient instability can be affected by uncertainty in, or small changes to, entries in the community matrix, and determine lower and upper bounds to the maximum amplitude of perturbations to the population vector. Of five different types of community matrix, we find that amplification is least severe when predator-prey interactions dominate. This analysis is relevant to other systems whose dynamics can be expressed in terms of the Jacobian matrix.

The ghost of nestedness in ecological networks.

Ecologists are fascinated by the prevalence of nestedness in biogeographic and community data, where it is thought to promote biodiversity in mutualistic systems. Traditionally, nestedness has been treated in a binary sense: species and their interactions are either present or absent, neglecting information on abundances and interaction frequencies. Extending nestedness to quantitative data facilitates the study of species preferences, and we propose a new detection method that follows from a basic property of bipartite networks: large dominant eigenvalues are associated with highly nested configurations. We show that complex ecological networks are binary nested, but quantitative preferences are non-nested, indicating limited consumer overlap of favoured resources. The spectral graph approach provides a formal link to local dynamical stability analysis, where we demonstrate that nested mutualistic structures are minimally stable. We conclude that, within the binary constraint of interaction plausibility, species preferences are partitioned to avoid competition, thereby benefiting system-wide resource allocation.

Warming and nitrogen affect size structuring and density dependence in a host-parasitoid food web.

Body size is a major factor constraining the trophic structure and functioning of ecological communities. Food webs are known to respond to changes in basal resource abundance, and climate change can initiate compounding bottom-up effects on food-web structure through altered resource availability and quality. However, the effects of climate and co-occurring global changes, such as nitrogen deposition, on the density and size relationships between resources and consumers are unknown, particularly in host-parasitoid food webs, where size structuring is less apparent. We use a Bayesian modelling approach to explore the role of consumer and resource density and body size on host-parasitoid food webs assembled from a field experiment with factorial warming and nitrogen treatments. We show that the treatments increased resource (host) availability and quality (size), leading to measureable changes in parasitoid feeding behaviour. Parasitoids interacted less evenly within their host range and increasingly focused on abundant and high-quality (i.e. larger) hosts. In summary, we present evidence that climate-mediated bottom-up effects can significantly alter food-web structure through both density- and trait-mediated effects.

Structural dynamics and robustness of food webs.

Food web structure plays an important role when determining robustness to cascading secondary extinctions. However, existing food web models do not take into account likely changes in trophic interactions ('rewiring') following species loss. We investigated structural dynamics in 12 empirically documented food webs by simulating primary species loss using three realistic removal criteria, and measured robustness in terms of subsequent secondary extinctions. In our model, novel trophic interactions can be established between predators and food items not previously consumed following the loss of competing predator species. By considering the increase in robustness conferred through rewiring, we identify a new category of species--overlap species--which promote robustness as shown by comparing simulations incorporating structural dynamics to those with static topologies. The fraction of overlap species in a food web is highly correlated with this increase in robustness; whereas species richness and connectance are uncorrelated with increased robustness. Our findings underline the importance of compensatory mechanisms that may buffer ecosystems against environmental change, and highlight the likely role of particular species that are expected to facilitate this buffering.