The Robustness of Plant-Pollinator Assemblages: Linking Plant Interaction Patterns and Sensitivity to Pollinator Loss

Most flowering plants depend on pollinators to reproduce. Thus, evaluating the robustness of plant-pollinator assemblages to species loss is a major concern. How species interaction patterns are related to species sensitivity to partner loss may influence the robustness of plant-pollinator assemblages. In plants, both reproductive dependence on pollinators (breeding system) and dispersal ability may modulate plant sensitivity to pollinator loss. For instance, species with strong dependence (e.g. dioecious species) and low dispersal (e.g. seeds dispersed by gravity) may be the most sensitive to pollinator loss. We compared the interaction patterns of plants differing in dependence on pollinators and dispersal ability in a meta-dataset comprising 192 plant species from 13 plant-pollinator networks. In addition, network robustness was compared under different scenarios representing sequences of plant extinctions associated with plant sensitivity to pollinator loss. Species with different dependence on pollinators and dispersal ability showed similar levels of generalization. Although plants with low dispersal ability interacted with more generalized pollinators, low-dispersal plants with strong dependence on pollinators (i.e. the most sensitive to pollinator loss) interacted with more particular sets of pollinators (i.e. shared a low proportion of pollinators with other plants). Only two assemblages showed lower robustness under the scenario considering plant generalization, dependence on pollinators and dispersal ability than under the scenario where extinction sequences only depended on plant generalization (i.e. where higher generalization level was associated with lower probability of extinction). Overall, our results support the idea that species generalization and network topology may be good predictors of assemblage robustness to species loss, independently of plant dispersal ability and breeding system. In contrast, since ecological specialization among partners may increase the probability of disruption of interactions, the fact that the plants most sensitive to pollinator loss interacted with more particular pollinator assemblages suggest that the persistence of these plants and their pollinators might be highly compromised.     

Conspecific and Heterospecific Plant Densities at Small-Scale Can Drive Plant-Pollinator Interactions

Generalist pollinators are important in many habitats, but little research has been done on small-scale spatial variation in interactions between them and the plants that they visit. Here, using a spatially explicit approach, we examined whether multiple species of flowering plants occurring within a single meadow showed spatial structure in their generalist pollinator assemblages.We report the results for eight plant species for which at least 200 individual visits were recorded. We found that for all of these species, the proportions of their general pollinator assemblages accounted for by particular functional groups showed spatial heterogeneity at the scale of tens of metres. This heterogeneity was connected either with no or only subtle changes of vegetation and flowering species composition. In five of these species, differences in conspecific plant density influenced the pollinator communities (with greater dominance of main pollinators at low-conspecific plant densities). The density of heterospecific plant individuals influenced the pollinator spectrum in one case.Our results indicate that the picture of plant-pollinator interactions provided by averaging data within large plots may be misleading and that within-site spatial heterogeneity should be accounted for in terms of sampling effort allocation and analysis. Moreover, spatially structured plant-pollinator interactions may have important ecological and evolutionary consequences, especially for plant population biology.     

Traits and phylogenetic history contribute to network structure across Canadian plant–pollinator communities

Interaction webs, or networks, define how the members of two or more trophic levels interact. However, the traits that mediate network structure have not been widely investigated. Generally, the mechanism that determines plant-pollinator partnerships is thought to involve the matching of a suite of species traits (such as abundance, phenology, morphology) between trophic levels. These traits are often unknown or hard to measure, but may reflect phylogenetic history. We asked whether morphological traits or phylogenetic history were more important in mediating network structure in mutualistic plant-pollinator interaction networks from Western Canada. At the plant species level, sexual system, growth form, and flower symmetry were the most important traits. For example species with radially symmetrical flowers had more connections within their modules (a subset of species that interact more among one another than outside of the module) than species with bilaterally symmetrical flowers. At the pollinator species level, social species had more connections within and among modules. In addition, larger pollinators tended to be more specialized. As traits mediate interactions and have a phylogenetic signal, we found that phylogenetically close species tend to interact with a similar set of species. At the network level, patterns were weak, but we found increasing functional trait and phylogenetic diversity of plants associated with increased weighted nestedness. These results provide evidence that both specific traits and phylogenetic history can contribute to the nature of mutualistic interactions within networks, but they explain less variation between networks.     

Non‐random patterns of invasion and extinction reduce phylogenetic diversity in island bird assemblages

Anthropogenically driven changes in bird communities on oceanic islands exemplify the biotic upheaval experienced by island floras and faunas. While the influence of invasions and extinctions on species richness and beta‐diversity of island bird assemblages has been explored, little is known about the impact of these invasions and extinctions on phylogenetic diversity. Here we quantify phylogenetic diversity of island bird assemblages resulting from extinctions alone, invasions alone, and the combination of extinctions and invasions in the historic time period (1500 CE to the current), and compare it to the expected phylogenetic diversity that would result if these processes involved randomly selected island bird species. We assessed phylogenetic diversity and structure at the scale of the island (n = 152), the archipelago containing the islands (n = 22), and the four oceans containing the archipelagos using three measures. We found that extinction, invasion, and the combination of invasion and extinction generally resulted in lower phylogenetic diversity than expected, regardless of the spatial scale examined. We conclude that extinction and invasion of birds on islands are non‐random with respect to phylogeny and that these processes generally leave bird assemblages with lower phylogenetic diversity than we would expect under random invasion or extinction.     

Trophically unique species are vulnerable to cascading extinction

Understanding which species might become extinct and the consequences of such loss is critical. One consequence is a cascade of further, secondary extinctions. While a significant amount is known about the types of communities and species that suffer secondary extinctions, little is known about the consequences of secondary extinctions for biodiversity. Here we examine the effect of these secondary extinctions on trophic diversity, the range of trophic roles played by the species in a community. Our analyses of natural and model food webs show that secondary extinctions cause loss of trophic diversity greater than that expected from chance, a result that is robust to variation in food web structure, distribution of interactions strengths, functional response, and adaptive foraging. Greater than expected loss of trophic diversity occurs because more trophically unique species are more vulnerable to secondary extinction. This is not a straightforward consequence of these species having few links with others but is a complex function of how direct and indirect interactions affect species persistence. A positive correlation between a species' extinction probability and the importance of its loss defines high-risk species and should make their conservation a priority.     

Population dynamics of plant and pollinator communities: stability reconsidered

Plant-pollinator networks are systems of outstanding ecological and economic importance. A particularly intriguing aspect of these systems is their high diversity. However, earlier studies have concluded that the specific mechanisms of plant-pollinator interactions are destabilizing and should lead to a loss of diversity. Here we present a mechanistic model of plant and pollinator population dynamics with the ability to represent a broad spectrum of interaction structures. Using this model, we examined the influence of pollinators on the stability of a plant community and the relationship between pollinator specialization and stability. In accordance with earlier work, our results show that plant-pollinator interactions may severely destabilize plant coexistence, regardless of the degree of pollinator specialization. However, if plant niche differentiation, a classical stabilizing mechanism, is sufficiently strong to overcome the minority disadvantage with respect to pollination, interactions with pollinators may even increase the stability of a plant community. In addition to plant niche differentiation, the relationship between specialization and stability depends on a number of parameters that affect pollinator growth rates. Our results highlight the complex effects of this particular type of mutualism on community stability and call for further investigations of the mechanisms of diversity maintenance in plant-pollinator systems.     

Plant traits and landscape simplification drive intraspecific trait diversity of Bombus terrestris in wildflower plantings

Wildflower plantings are an important mitigation tool within agri-environmental schemes to counter insect decline in resource-scarce agricultural landscapes. Effectiveness of wildflower plantings for insect conservation is typically studied at the community or species level. It is the individual, however, that is subject to changing abiotic and biotic conditions, not the species per se. Accordingly, functional traits of individuals, i.e., the intraspecific functional diversity within species, likely mediate responses to wildflower resources and landscape context. Here we focused on the ecologically and economically important wild insect pollinator Bombus terrestris to study its intraspecific functional diversity and plant-pollinator individual interactions in wildflower plantings. We found considerable trait variation among flower-visiting B. terrestris workers. Locally, this variation could be attributed to flowering plant traits, with larger workers visiting larger inflorescences and individuals with longer tongues preferentially feeding on zygomorphic but not radially symmetrical flowers. In addition, wildflower plantings with high floral abundance attracted individuals with larger pollen baskets. At the landscape scale, increasing proportion of arable land resulted in smaller B. terrestris individuals in wildflower plantings, and a decrease in the overall size diversity of workers. These findings highlight the so far little considered role of intraspecific variation in functional traits of wild pollinators, which can mediate the trait-matching between plants and pollinator individuals. Landscape simplification from agriculture threatens intraspecific pollinator diversity, with potential harmful effects for pollinator fitness and plant reproduction. Tailored wildflower plantings can thus serve as an important tool to increase intraspecific variation in simplified landscapes. When designing seed mixtures for these plantings, high complementarity in plant traits is key for promoting high intraspecific trait diversity of bumblebees and potentially of other associated insect species.     

Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness

Biotic and abiotic factors may individually or interactively disrupt plant–pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant–pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant–pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.     

Phylogenetic Community Context Influences Pollen Delivery to <Emphasis Type="Italic">Allium cernuum</Emphasis>

Few studies have examined how the number and identity of species in the neighbouring community influences the reproductive success of particular focal species. Pollen delivery, an important component of fitness of sexual plants, is a function of not just the floral traits of any particular individual, but of features of the population and community as it depends on pollinator abundance and preferences. Many pollinators in flowering communities will prefer patches with high floral abundance or diversity yet may exhibit lower floral constancy when more flowering species are present. Thus, pollination efficiency could increase or decrease with increased species richness and this will alter the selection pressures placed upon the floral traits (such as floral colour or reward) of any member of a particular community. Moreover, recent studies have indicated that plant-pollinator networks are phylogenetically structured (pollinators visit related plant species more than expected by chance) and this may be an important factor structuring flowering plant communities. Thus, the sheer number of species within a patch may be less important than the number of closely-related species. We investigate whether species richness or phylogenetic proximity of coflowering species influences the amount and proportion of conspecific pollen delivered to nodding onion, Allium cernuum, in fragment patches of Garry Oak meadows in South Western British Columbia, Canada. We find that pollen delivery depended upon the presence of close relatives far more than on species richness or population density, indicating a central role of the community structure on pollination in flowering plant communities. Insofar as pollen delivery relates to the relative number of seeds produced by members of the community, pollination may in turn determine the community structure of the next generation.     

Uni-directional Interaction and Plant–Pollinator–Robber Coexistence

A mathematical model for the plant-pollinator-robber interaction is studied to understand the factors leading to the widespread occurrence and stability of such interactions. In the interaction, a flowering plant provides resource for its pollinator and the pollinator has both positive and negative effects on the plant. A nectar robber acts as a plant predator, consuming a common resource with the pollinator, but with a different functional response. Using dynamical systems theory, mechanisms of species coexistence are investigated to show how a robber could invade the plant-pollinator system and persist stably with the pollinator. In addition, circumstances are demonstrated in which the pollinator's positive and negative effects on the plant could determine the robber's invasibility and the three-species coexistence.     

Plant generalization on pollinators: species property or local phenomenon?

Despite recent increased interest in the frequency and evolutionary consequences of generalization in plant-pollinator systems, little is known on whether plant generalization on pollinators actually is a species-level trait. This paper addresses the following questions for the insect-pollinated shrub Lavandula latifolia: (1) Are different populations of this pollinator-generalist plant similarly generalized? (2) Within a highly generalized population, are all plants similarly pollinator-generalists? Comparable values for richness in pollinator species were obtained from individual- or population-specific rarefaction curves as the projected number of distinct pollinator species implicated in 100 flower visits (S(RAR100)). Simple counts of pollinator species recorded per individual or population (S(OBS)) were weakly or nonsignificantly correlated with corresponding S(RAR100) figures and closely correlated with flower visitation frequency. The pollination system of L. latifolia was highly generalized at the regional level, but populations differed greatly in pollinator species richness (S(RAR100)). Within the population intensively studied, individual plants had quite variable degrees of generalization, comparable in magnitude to variation among populations. It is concluded that generalization was not an invariant, species-level property in L. latifolia. Furthermore, pollinator diversity estimates based on S(OBS) data may be heavily contingent on aspects related to both research design (sampling effort) and biological phenomena (variation in pollinator abundance or visitation rates), which may either mask or distort underlying ecological patterns of interest.     

Decoupled responses of biodiversity facets driven from anuran vulnerability to climate and land-use changes

Biodiversity loss not only implies the loss of species but also entails losses in other dimensions of biodiversity, such as functional, phylogenetic and interaction diversity. Yet, each of those facets of biodiversity may respond differently to extinctions. Here, we examine how extinction, driven by climate and land-use changes may affect those different facets of diversity by combining empirical data on anuran–prey interaction networks, species distribution modelling and extinction simulations in assemblages representing four Neotropical ecoregions. We found a mismatch in the response of functional, phylogenetic and interaction diversity to extinction. In spite of high network robustness to extinction, the effects on interaction diversity were stronger than those on phylogenetic and functional diversity, declining linearly with species loss. Although it is often assumed that interaction patterns are reflected by functional diversity, assessing species interactions may be necessary to understand how species loss translates into the loss of ecosystem functions.     

Phylogenetic restriction of plant invasion in drought‐stressed environments: Implications for insect‐pollinated plant communities in water‐limited ecosystems

BackgroundPlant–pollinator community diversity has been found to decrease under conditions of drought stress; however, research into the temporal dimensions of this phenomenon remains limited. In this study, we investigated the effect of seasonal drought on the temporal niche dynamics of entomophilous flowering plants in a water‐limited ecosystem. We hypothesized that closely related native and exotic plants would tend to share similar life history and that peak flowering events would therefore coincide with phylogenetic clustering in plant communities based on expected phenological responses of plant functional types to limitations in soil moisture availability.LocationGaliano Island, British Columbia, Canada.MethodsCombining methods from pollinator research and phylogenetic community ecology, we tested the influence of environmental filtering over plant community phenology across gradients of landscape disturbance and soil moisture. Floral resource availability and community structure were quantified by counts of flowering shoots. We constructed a robust phylogeny to analyze spatial and temporal variation in phylogenetic patterns across the landscape, testing the significance of the observed patterns against a randomly generated community phylogeny. Phylogenetic metrics were then regressed against factors of disturbance and soil moisture availability.ResultsCritical seasonal fluctuations in floral resources coincided with significant phylogenetic clustering in plant communities, with decreasing plant diversity observed under conditions of increasing drought stress. Exotic plant species in the Asteraceae became increasingly pervasive across the landscape, occupying a late season temporal niche in drought‐stressed environments.Main conclusionResults suggest that environmental filtering is the dominant assembly process structuring the temporal niche of plant communities in this water‐limited ecosystem. Based on these results, and trends seen elsewhere, the overall diversity of plant–pollinator communities may be expected to decline with the increasing drought stress predicted under future climate scenarios.     

Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities

Pollination is exclusively or mainly animal mediated for 70% to 90% of angiosperm species. Thus, pollinators provide an essential ecosystem service to humankind. However, the impact of human-induced biodiversity loss on the functioning of plant–pollinator interactions has not been tested experimentally. To understand how plant communities respond to diversity changes in their pollinating fauna, we manipulated the functional diversity of both plants and pollinators under natural conditions. Increasing the functional diversity of both plants and pollinators led to the recruitment of more diverse plant communities. After two years the plant communities pollinated by the most functionally diverse pollinator assemblage contained about 50% more plant species than did plant communities pollinated by less-diverse pollinator assemblages. Moreover, the positive effect of functional diversity was explained by a complementarity between functional groups of pollinators and plants. Thus, the functional diversity of pollination networks may be critical to ecosystem sustainability.     

Functional Diversity of Plant–Pollinator Interaction Webs Enhances the Persistence of Plant Communities

Pollination is exclusively or mainly animal mediated for 70% to 90% of angiosperm species. Thus, pollinators provide an essential ecosystem service to humankind. However, the impact of human-induced biodiversity loss on the functioning of plant–pollinator interactions has not been tested experimentally. To understand how plant communities respond to diversity changes in their pollinating fauna, we manipulated the functional diversity of both plants and pollinators under natural conditions. Increasing the functional diversity of both plants and pollinators led to the recruitment of more diverse plant communities. After two years the plant communities pollinated by the most functionally diverse pollinator assemblage contained about 50% more plant species than did plant communities pollinated by less-diverse pollinator assemblages. Moreover, the positive effect of functional diversity was explained by a complementarity between functional groups of pollinators and plants. Thus, the functional diversity of pollination networks may be critical to ecosystem sustainability.     

Global warming and the disruption of plant-pollinator interactions

Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO₂. Depending on model assumptions, phenological shifts reduced the floral resources available to 17–50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.     

Diverse pollinator communities enhance plant reproductive success

Understanding the functional consequences of biodiversity loss is a major goal of ecology. Animal-mediated pollination is an essential ecosystem function and service provided to mankind. However, little is known how pollinator diversity could affect pollination services. Using a substitutive design, we experimentally manipulated functional group (FG) and species richness of pollinator communities to investigate their consequences on the reproductive success of an obligate out-crossing model plant species, Raphanus sativus. Both fruit and seed set increased with pollinator FG richness. Furthermore, seed set increased with species richness in pollinator communities composed of a single FG. However, in multiple-FG communities, highest species richness resulted in slightly reduced pollination services compared with intermediate species richness. Our analysis indicates that the presence of social bees, which showed roughly four times higher visitation rates than solitary bees or hoverflies, was an important factor contributing to the positive pollinator diversity–pollination service relationship, in particular, for fruit set. Visitation rate at different daytimes, and less so among flower heights, varied among social bees, solitary bees and hoverflies, indicating a niche complementarity among these pollinator groups. Our study demonstrates enhanced pollination services of diverse pollinator communities at the plant population level and suggests that both the niche complementarity and the presence of specific taxa in a pollinator community drive this positive relationship.     

Pollinator type and secondarily climate are related to nectar sugar composition across the angiosperms

Pollinators are important agents of selection on floral traits, including nectar sugar composition. Although it is widely assumed that the proportion of sugars (mainly sucrose, glucose and fructose) in nectar reflects pollinators’ physiological limitations and digestive efficiency, the relative impact of pollinators and abiotic factors on nectar sugar composition, as well as the generality of these associations across the angiosperms, remain unknown. We compiled data on nectar sugar composition for >1000 plant species, along with information on flower visitors, plant growth form and latitudinal climatic zone, to provide the first comprehensive assessment of correlates of variation in sugar nectar composition in the angiosperms. After assembling a phylogeny linking all species in the dataset, we estimated the amount of phylogenetic signal in the percentage of sucrose and, by applying phylogenetically-informed multiple regressions, we evaluated whether nectar composition was influenced either by the main pollinator group, plant growth form, or latitudinal climatic zone. The relative importance of each of these factors was then assessed through model selection based on Akaike information criteria and deviance partitioning analysis. Nectar was dominated by sucrose in 56.8% of all the species, glucose in 16.7%, and fructose in 5.5%. Nectar in the remaining species was characterized by similar proportions of the three sugars. Variation in the proportion of sucrose was highest (~70%) at the intrafamily level, and had a significant but low phylogenetic signal, which partially reflects phylogenetic conservatism of the pollinator niche. After controlling for phylogenetic effects, the proportion of sucrose was mainly related to pollinator type and secondarily to climate. Accordingly, this study indicates that nectar sugar composition shows high evolutionary lability and its variation reflects plant-pollinator associations.     

A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance

Understanding and predicting species extinctions and coextinctions is a major goal of ecological research in the face of a biodiversity crisis. Typically, models based on network topology are used to simulate coextinctions in mutualistic networks. However, such topological models neglect two key biological features of species interactions: variation in the intrinsic dependence of species on the mutualism, and variation in the relative importance of each interacting partner. By incorporating both types of variation, we developed a stochastic coextinction model capable of simulating extinction cascades far more complex than those observed in previous topological models. Using a set of empirical mutualistic networks, we show that the traditional topological model may either underestimate or overestimate the number and likelihood of coextinctions, depending on the intrinsic dependence of species on the mutualism. More importantly, contrary to topological models, our stochastic model predicts extinction cascades to be more likely in highly connected mutualistic communities.