Using individual-based trait frequency distributions to forecast plant-pollinator network responses to environmental change.

Determining how and why organisms interact is fundamental to understanding ecosystem responses to future environmental change. To assess the impact on plant-pollinator interactions, recent studies have examined how the effects of environmental change on individual interactions accumulate to generate species-level responses. Here, we review recent developments in using plant-pollinator networks of interacting individuals along with their functional traits, where individuals are nested within species nodes. We highlight how these individual-level, trait-based networks connect intraspecific trait variation (as frequency distributions of multiple traits) with dynamic responses within plant-pollinator communities. This approach can better explain interaction plasticity, and changes to interaction probabilities and network structure over spatiotemporal or other environmental gradients. We argue that only through appreciating such trait-based interaction plasticity can we accurately forecast the potential vulnerability of interactions to future environmental change. We follow this with general guidance on how future studies can collect and analyse high-resolution interaction and trait data, with the hope of improving predictions of future plant-pollinator network responses for targeted and effective conservation.

Body-size-dependent effects of landscape-level resource energetics on pollinator abundance in woodland remnants.

Land use change alters floral resource availability, thereby contributing to declines in important pollinators. However, the severity of land use impact varies by species, influenced by factors such as dispersal ability and resource specialization, both of which can correlate with body size. Here. we test whether floral resource availability in the surrounding landscape (the 'matrix') influences bee species' abundance in isolated remnant woodlands, and whether this effect varies with body size. We sampled quantitative flower-visitation networks within woodland remnants and quantified floral energy resources (nectar and pollen calories) available to each bee species both within the woodland and the matrix. Bee abundance in woodland increased with floral energy resources in the surrounding matrix, with strongest effects on larger-bodied species. Our findings suggest important but size-dependent effects of declining matrix floral resources on the persistence of bees in remnant woodlands, highlighting the need to incorporate landscape-level floral resources in conservation planning for pollinators in threatened natural habitats.

Root diameter, host specificity and arbuscular mycorrhizal fungal community composition among native and exotic plant species.

Plant root systems rely on a functionally diverse range of arbuscular mycorrhizal fungi to, among other benefits, extend their nutrient foraging. Extended nutrient foraging is likely of greatest importance to coarse-rooted plants, yet few studies have examined the link between root traits and arbuscular mycorrhizal fungal community composition. Here, we examine the relationship between root diameter and the composition of arbuscular mycorrhizal fungal communities in a range of native and exotic plant species. We characterized the arbuscular mycorrhizal fungal communities of 30 co-occurring native and exotic montane grassland/shrubland plant species in New Zealand. We found that plant root diameter and native/exotic status both strongly correlated with arbuscular mycorrhizal fungal community composition. Coarse-rooted plants had a lower diversity of mycorrhizal fungi compared with fine-rooted plants and associated less with generalist fungal partners. Exotic plants had a lower diversity of fungi and fewer associations with nondominant families of arbuscular mycorrhizal fungi compared with native plants. These observational patterns suggest that plants may differentially associate with fungal partners based on their root traits, with coarse-rooted plants being more specific in their associations. Furthermore, exotic plants may associate with dominant arbuscular mycorrhizal fungal taxa as a strategy in invasion.

Behaviour moderates the impacts of food-web structure on species coexistence.

How species coexistence (mathematical 'feasibility') in food webs emerges from species' trophic interactions remains a long-standing open question. Here we investigate how structure (network topology and body-size structure) and behaviour (foraging strategy and spatial dimensionality of interactions) interactively affect feasibility in food webs. Metabolically-constrained modelling of food-web dynamics based on whole-organism consumption revealed that feasibility is promoted in systems dominated by large-eat-small foraging (consumers eating smaller resources) whenever (1) many top consumers are present, (2) grazing or sit-and-wait foraging strategies are common, and (3) species engage in two-dimensional interactions. Congruently, the first two conditions were associated with dominance of large-eat-small foraging in 74 well-resolved (primarily aquatic) real-world food webs. Our findings provide a new, mechanistic understanding of how behavioural properties can modulate the effects of structural properties on species coexistence in food webs, and suggest that 'being feasible' constrains the spectra of behavioural and structural properties seen in natural food webs.

Trait matching and phenological overlap increase the spatio-temporal stability and functionality of plant-pollinator interactions.

Morphology and phenology influence plant-pollinator network structure, but whether they generate more stable pairwise interactions with higher pollination success remains unknown. Here we evaluate the importance of morphological trait matching, phenological overlap and specialisation for the spatio-temporal stability (measured as variability) of plant-pollinator interactions and for pollination success, while controlling for species' abundance. To this end, we combined a 6-year plant-pollinator interaction dataset, with information on species traits, phenologies, specialisation, abundance and pollination success, into structural equation models. Interactions among abundant plants and pollinators with well-matched traits and phenologies formed the stable and functional backbone of the pollination network, whereas poorly matched interactions were variable in time and had lower pollination success. We conclude that phenological overlap could be more useful for predicting changes in species interactions than species abundances, and that non-random extinction of species with well-matched traits could decrease the stability of interactions within communities and reduce their functioning.

Strength of niche processes for species interactions is lower for generalists and exotic species.

Niche and neutral processes jointly influence species interactions. Predictions of interactions based on these processes assume that they operate similarly across all species. However, species characteristics could systematically create differences in the strength of niche or neutral processes for each interspecific interaction. We used national-level records of plant-frugivore interactions, species traits, biogeographic status (native vs. exotic), phylogenies and species range sizes to test the hypothesis that the strength of niche processes in species interactions changes in predictable ways depending on trophic generalism and biogeographic status of the interacting species. The strength of niche processes (measured as trait matching) decreased when the generalism of the interacting partners increased. Furthermore, the slope of this negative relationship between trait matching and generalism of the interacting partners was steeper (more negative) for interactions between exotic species than those between native species. These results remained significant after accounting for the potential effects of neutral processes (estimated by species range size). These observed changes in the strength of niche processes in generating species interactions, after accounting for effects of neutral processes, could improve predictions of ecological networks from species trait data. Specifically, due to their shorter co-evolutionary history, exotic species tend to interact with native species even when lower trait matching occurs than in interactions among native species. Likewise, interactions between generalist bird species and generalist plant species should be expected to occur despite low trait matching between species, whereas interactions between specialist species involve higher trait matching.

Intensified agriculture favors evolved resistance to biological control.

Increased regulation of chemical pesticides and rapid evolution of pesticide resistance have increased calls for sustainable pest management. Biological control offers sustainable pest suppression, partly because evolution of resistance to predators and parasitoids is prevented by several factors (e.g., spatial or temporal refuges from attacks, reciprocal evolution by control agents, and contrasting selection pressures from other enemy species). However, evolution of resistance may become more probable as agricultural intensification reduces the availability of refuges and diversity of enemy species, or if control agents have genetic barriers to evolution. Here we use 21 y of field data from 196 sites across New Zealand to show that parasitism of a key pasture pest (Listronotus bonariensis; Argentine stem weevil) by an introduced parasitoid (Microctonus hyperodae) was initially nationally successful but then declined by 44% (leading to pasture damage of c. 160 million New Zealand dollars per annum). This decline was not attributable to parasitoid numbers released, elevation, or local climatic variables at sample locations. Rather, in all locations the decline began 7 y (14 host generations) following parasitoid introduction, despite releases being staggered across locations in different years. Finally, we demonstrate experimentally that declining parasitism rates occurred in ryegrass Lolium perenne, which is grown nationwide in high-intensity was significantly less than in adjacent plots of a less-common pasture grass (Lolium multiflorum), indicating that resistance to parasitism is host plant-dependent. We conclude that low plant and enemy biodiversity in intensive large-scale agriculture may facilitate the evolution of host resistance by pests and threaten the long-term viability of biological control.

Predation risk influences food-web structure by constraining species diet choice.

The foraging behaviour of species determines their diet and, therefore, also emergent food-web structure. Optimal foraging theory (OFT) has previously been applied to understand the emergence of food-web structure through a consumer-centric consideration of diet choice. However, the resource-centric viewpoint, where species adjust their behaviour to reduce the risk of predation, has not been considered. We develop a mechanistic model that merges metabolic theory with OFT to incorporate the effect of predation risk on diet choice to assemble food webs. This 'predation-risk-compromise' (PR) model better captures the nestedness and modularity of empirical food webs relative to the classical optimal foraging model. Specifically, compared with optimal foraging alone, risk-mitigated foraging leads to more-nested but less-modular webs by broadening the diet of consumers at intermediate trophic levels. Thus, predation risk significantly affects food-web structure by constraining species' ability to forage optimally, and needs to be considered in future work.

Reshaping our understanding of species' roles in landscape-scale networks.

In network ecology, landscape-scale processes are often overlooked, yet there is increasing evidence that species and interactions spill over between habitats, calling for further study of interhabitat dependencies. Here, we investigate how species connect a mosaic of habitats based on the spatial variation of their mutualistic and antagonistic interactions using two multilayer networks, combining pollination, herbivory and parasitism in the UK and New Zealand. Developing novel methods of network analysis for landscape-scale ecological networks, we discovered that few plant and pollinator species acted as connectors or hubs, both within and among habitats, whereas herbivores and parasitoids typically have more peripheral network roles. Insect species' roles depend on factors other than just the abundance of taxa in the lower trophic level, exemplified by larger Hymenoptera connecting networks of different habitats and insects relying on different resources across different habitats. Our findings provide a broader perspective for landscape-scale management and ecological community conservation.

Symmetric assembly and disassembly processes in an ecological network.

The processes whereby ecological networks emerge, persist and decay throughout ecosystem development are largely unknown. Here we study networks of plant and arbuscular mycorrhizal fungal (AMF) communities along a 120 000 year soil chronosequence, as they undergo assembly (progression) and then disassembly (retrogression). We found that network assembly and disassembly were symmetrical, self-reinforcing processes that together were capable of generating key attributes of network architecture. Plant and AMF species that had short indirect paths to others in the community (i.e. high centrality), rather than many direct interaction partners (i.e. high degree), were best able to attract new interaction partners and, in the case of AMF species, also to retain existing interactions with plants during retrogression. We then show using simulations that these non-random patterns of attachment and detachment promote nestedness of the network. These results have implications for predicting extinction sequences, identifying focal points for invasions and suggesting trajectories for restoration.

Dung beetle-mediated soil modification: a data set for analyzing the effects of a recent introduction on soil quality.

Globally, dung beetles (Scarabaeidae: Scarabaeinae) are linked to many critical ecosystem processes involving the consumption and breakdown of mammal dung. Due to New Zealand's unique evolutionary history, resulting from its geographic isolation from Gondwana, endemic dung-dwelling fauna evolved in the absence of large mammals. Europeans introduced livestock to the islands in the late 18th and 19th centuries, resulting in a buildup of undecomposed feces and unrecycled nutrients due to the absence of dung beetles. To mitigate this situation, in 2011, the New Zealand Environmental Protection Agency approved the release of 11 species of exotic beetles with the expectation that these insects would fulfill a critically missing link in converting aboveground manure biomass into higher quality soils belowground. Widespread releases began in 2014. To enable others in the future to test the environmental impacts of the beetle introductions, we present a detailed characterization of soil physical, chemical, and biological properties, shortly after the initial and intentional introduction of dung beetles to 16 release sites across both the North and South Islands of New Zealand. As beetle populations become established, these baseline data will enable quantification of the degree to which different exotic dung beetle communities can modify soils, specifically if they facilitate soil nutrient cycling. There are no copyright or proprietary restrictions for research or teaching purposes. Usage of the data set must be cited by referencing this publication.

Non-random food-web assembly at habitat edges increases connectivity and functional redundancy.

Habitat fragmentation dramatically alters the spatial configuration of landscapes, with the creation of artificial edges affecting community structure and dynamics. Despite this, it is not known how the different food webs in adjacent habitats assemble at their boundaries. Here we demonstrate that the composition and structure of herbivore-parasitoid food webs across edges between native and plantation forests are not randomly assembled from those of the adjacent communities. Rather, elevated proportions of abundant, interaction-generalist parasitoid species at habitat edges allowed considerable interaction rewiring, which led to higher linkage density and less modular networks, with higher parasitoid functional redundancy. This was despite high overlap in host composition between edges and interiors. We also provide testable hypotheses for how food webs may assemble between habitats with lower species overlap. In an increasingly fragmented world, non-random assembly of food webs at edges may increasingly affect community dynamics at the landscape level.

Linking species functional roles to their network roles.

Species roles in ecological networks combine to generate their architecture, which contributes to their stability. Species trait diversity also affects ecosystem functioning and resilience, yet it remains unknown whether species' contributions to functional diversity relate to their network roles. Here, we use 21 empirical pollen transport networks to characterise this relationship. We found that, apart from a few abundant species, pollinators with original traits either had few interaction partners or interacted most frequently with a subset of these partners. This suggests that narrowing of interactions to a subset of the plant community accompanies pollinator niche specialisation, congruent with our hypothesised trade-off between having unique traits vs. being able to interact with many mutualist partners. Conversely, these effects were not detected in plants, potentially because key aspects of their flowering traits are conserved at a family level. Relating functional and network roles can provide further insight into mechanisms underlying ecosystem functioning.

Persist or Produce: A Community Trade-Off Tuned by Species Evenness.

Understanding the effects of biodiversity on community persistence and productivity is key to managing both natural and production systems. Because rare species face greater danger of extinction, species evenness, a measure of how similar abundances are across species in a community, is seen as a key component of biodiversity. However, previous studies have failed to find a consistent association of species evenness with species survival and biomass production. Here we provide a theoretical framework for the relationship among these three elements. We demonstrate that the lack of consistent outcomes is not an idiosyncratic artifact of different studies but can be unified under one common framework. Applying a niche theory approach, we confirm that under demographic stochasticity evenness is a general indicator of the risk of future species extinctions in a community, in accordance with the majority of empirical studies. In contrast, evenness cannot be used as a direct indicator of the level of biomass production in a community. When a single species dominates, as expressed by the constraints imposed by the population dynamics, biomass production depends on the niche position of the dominating species and can increase or decrease with evenness. We demonstrate that high species evenness and an intermediate level of biomass production is the configuration that maximizes the average species survival probability in response to demographic stochasticity.

Microbes in the Anthropocene: spillover of agriculturally selected bacteria and their impact on natural ecosystems.

Soil microbial communities are enormously diverse, with at least millions of species and trillions of genes unknown to science or poorly described. Soil microbial communities are key components of agriculture, for example, in provisioning nitrogen and protecting crops from pathogens, providing overall ecosystem services in excess of $1000bn per year. It is important to know how humans are affecting this hidden diversity. Much is known about the negative consequences of agricultural intensification on higher organisms, but almost nothing is known about how alterations to landscapes affect microbial diversity, distributions and processes. We review what is known about spatial flows of microbes and their response to land-use change, and outline nine hypotheses to advance research of microbiomes across landscapes. We hypothesize that intensified agriculture selects for certain taxa and genes, which then 'spill over' into adjacent unmodified areas and generate a halo of genetic differentiation around agricultural fields. Consequently, the spatial configuration and management intensity of different habitats combines with the dispersal ability of individual taxa to determine the extent of spillover, which can impact the functioning of adjacent unmodified habitats. When landscapes are heterogeneous and dispersal rates are high, this will select for large genomes that allow exploitation of multiple habitats, a process that may be accelerated through horizontal gene transfer. Continued expansion of agriculture will increase genotypic similarity, making microbial community functioning increasingly variable in human-dominated landscapes, potentially also impacting the consistent provisioning of ecosystem services. While the resulting economic costs have not been calculated, it is clear that dispersal dynamics of microbes should be taken into consideration to ensure that ecosystem functioning and services are maintained in agri-ecosystem mosaics.

Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development.

Little is known about the response of arbuscular mycorrhizal fungal communities to ecosystem development. We use a long-term soil chronosequence that includes ecosystem progression and retrogression to quantify the importance of host plant identity as a factor driving fungal community composition during ecosystem development. We identified arbuscular mycorrhizal fungi and plant species from 50 individual roots from each of 10 sites spanning 5-120 000 yr of ecosystem age using terminal restriction fragment length polymorphism (T-RFLP), Sanger sequencing and pyrosequencing. Arbuscular mycorrhizal fungal communities were highly structured by ecosystem age. There was strong niche differentiation, with different groups of operational taxonomic units (OTUs) being characteristic of early succession, ecosystem progression and ecosystem retrogression. Fungal alpha diversity decreased with ecosystem age, whereas beta diversity was high at early stages and lower in subsequent stages. A total of 39% of the variance in fungal communities was explained by host plant and site age, 29% of which was attributed to host and the interaction between host and site (24% and 5%, respectively). The strong response of arbuscular mycorrhizal fungi to ecosystem development appears to be largely driven by plant host identity, supporting the concept that plant and fungal communities are tightly coupled rather than independently responding to habitat.

Community-level net spillover of natural enemies from managed to natural forest.

Edge effects in fragmented natural habitats may De exaceroateci by intensive land use in the surrounding landscape. Given that most managed systems have higher primary productivity than adjacent natural systems, theory suggests that bottom-up subsidized consumers are likely to spill over from managed to natural habitats. Furthermore, the magnitude of spillover is likely to differ between generalist and specialist consumers, because of differences in their ability to use the full spectrum of resources. However, it is unknown whether there is indeed asymmetrical spillover of consumers between managed and natural habitats, and whether this is related to resource abundance or the trophic specialization of the consumer. We used flight intercept traps to measure spillover of generalist predators (Vespula wasps, Vespidae) and more specialist predators (106 species of parasitoids, Ichneumonidae and Braconidae) across habitat edges between native New Zealand forest and exotic plantation forest over a summer season. We found net spillover of both generalist and specialist predators from plantation to native forest, and that this was greater for generalists. To test whether natural enemy spillover from managed habitats was related to prey (caterpillar) abundance (i.e., whether it was bottom-up productivity driven, due to increased primary productivity), we conducted a large-scale herbivore reduction experiment at half of our plantation sites, by helicopter spraying caterpillar-specific insecticide over 2.5 ha per site. We monitored bidirectional natural enemy spillover and found that herbivore reduction reduced generalist but not specialist predator spillover. Trophic generalists may benefit disproportionately from high resource productivity in a habitat, and their cross-habitat spillover effects on natural food webs may be an important source of consumer pressure in mosaic landscapes.

Phylogenetic diversity and co-evolutionary signals among trophic levels change across a habitat edge.

Incorporating the evolutionary history of species into community ecology enhances understanding of community composition, ecosystem functioning and responses to environmental changes. Phylogenetic history might partly explain the impact of fragmentation and land-use change on assemblages of interacting organisms and even determine potential cascading effects across trophic levels. However, it remains unclear whether phylogenetic diversity of basal resources is reflected at higher trophic levels in the food web. In particular, phylogenetic determinants of community structure have never been incorporated into habitat edge studies, even though edges are recognized as key factors affecting communities in fragmented landscapes. Here, we test whether phylogenetic diversity at different trophic levels (plants, herbivores and parasitoids) and signals of co-evolution (i.e. phylogenetic congruence) among interacting trophic levels change across an edge gradient between native and plantation forests. To ascertain whether there is a signal of co-evolution across trophic levels, we test whether related consumer species generally feed on related resource species. We found differences across trophic levels in how their phylogenetic diversity responded to the habitat edge gradient. Plant and native parasitoid phylogenetic diversity changed markedly across habitats, while phylogenetic variability of herbivores (which were predominantly native) did not change across habitats, though phylogenetic evenness declined in plantation interiors. Related herbivore species did not appear to feed disproportionately on related plant species (i.e. there was no signal of co-evolution) even when considering only native species, potentially due to the high trophic generality of herbivores. However, related native parasitoid species tended to feed on related herbivore species, suggesting the presence of a co-evolutionary signal at higher trophic levels. Moreover, this signal was stronger in plantation forests, indicating that this habitat may impose stresses on parasitoids that constrain them to attack only host species for which they are best adapted. Overall, changes in land use across native to plantation forest edges differentially affected phylogenetic diversity across trophic levels, and may also exert a strong selective pressure for particular co-evolved herbivore-parasitoid interactions.

Complementarity and redundancy of interactions enhance attack rates and spatial stability in host-parasitoid food webs.

Complementary resource use and redundancy of species that fulfill the same ecological role are two mechanisms that can respectively increase and stabilize process rates in ecosystems. For example, predator complementarity and redundancy can determine prey consumption rates and their stability, yet few studies take into account the multiple predator species attacking multiple prey at different rates in natural communities. Thus, it remains unclear whether these biodiversity mechanisms are important determinants of consumption in entire predator-prey assemblages, such that food-web interaction structure determines community-wide consumption and stability. Here, we use empirical quantitative food webs to study the community-wide effects of functional complementarity and redundancy of consumers (parasitoids) on herbivore control in temperate forests. We find that complementarity in host resource use by parasitoids was a strong predictor of absolute parasitism rates at the community level and that redundancy in host-use patterns stabilized community-wide parasitism rates in space, but not through time. These effects can potentially explain previous contradictory results from predator diversity research. Phylogenetic diversity (measured using taxonomic distance) did not explain functional complementarity or parasitism rates, so could not serve as a surrogate measure for functional complementarity. Our study shows that known mechanisms underpinning predator diversity effects on both functioning and stability can easily be extended to link food webs to ecosystem functioning.

Exotic birds increase generalization and compensate for native bird decline in plant-frugivore assemblages.

Exotic species are thought to alter the structure of natural communities and disrupt ecosystem functioning through invasion. Nevertheless, exotic species may also provide ecological insurance when they contribute to maintain ecosystem functions after the decline of native species following anthropogenic disturbance. Here, this hypothesis is tested with the assemblage of frugivorous birds and fleshy-fruited plants of New Zealand, which has suffered strong historical declines in native birds while simultaneously gaining new frugivores introduced by European settlers. We studied the plant-frugivore assemblage from measures of fruit and bird abundances and fruit consumption in nine forest patches, and tested how this changed across a gradient of relative abundance of exotic birds. We then examined how each bird species' role in the assemblage (the proportion of fruits and the number of plant species consumed) varied with their relative abundance, body size and native/exotic status. The more abundant and, to a lesser extent, larger birds species consumed a higher proportion of fruits from more plant species. Exotic birds consumed fruits less selectively and more proportionate to the local availability than did native species. Interaction networks in which exotic birds had a stronger role as frugivores had higher generalization, higher nestedness and higher redundancy of plants. Exotic birds maintained frugivory when native birds became rarer, and diversified the local spectrum of frugivores for co-occurring native plants. These effects seemed related to the fact that species abundances, rather than trait-matching constraints, ultimately determined the patterns of interactions between birds and plants. By altering the structure of plant-frugivore assemblages, exotic birds likely enhance the stability of the community-wide seed dispersal in the face of continued anthropogenic impact.