Structure of a plant-pollinator network on a pahoehoe lava desert of the Galápagos Islands

Plant-pollinator interactions are important for the evolution and survival of the species involved. Plant-pollinator networks on oceanic islands are often small in size and as a consequence the connectance is high suggesting a substantial generalisation level. Further, linkage level for insular plants is shown to be lower than on mainland. The present study investigates a plant-pollinator network on the Galápagos Islands that is unique because of its very small size. We recorded pollinator visits to plant species as well as pollen grains on insect bodies. The combination of these data increased the observed number of interactions. The values for connectance and linkage level for plants were found to be consistent with similar values found in other network studies. There were no relation between the abundance of plant species and the number of pollinating species. The dominating pollinator species was the Galápagos carpenter bee Xylocopa darwini . Specimens of the shorthorned grasshopper Halmenus cuspidatus turned out to carry pollen from five plant species out of twelve and are probably functioning as pollinator. Bagging experiments revealed dependency on insect visits for a high seed set for most of the plant species, but only one species Plumbago scandens seemed to possess a pollen limited seed set. The network showed an asymmetric pattern of number of interactions per species with a few species having several interactions and many species a few. This pattern is supposed to result in a rather robust community, but is also fairly sensitive if the dominant species are threatened. The high connectance value found could, however, counteract this vulnerability.     

Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization

We analysed the dynamics of a plant-pollinator interaction network of a scrub community surveyed over four consecutive years. Species composition within the annual networks showed high temporal variation. Temporal dynamics were also evident in the topology of the network, as interactions among plants and pollinators did not remain constant through time. This change involved both the number and the identity of interacting partners. Strikingly, few species and interactions were consistently present in all four annual plant-pollinator networks (53% of the plant species, 21% of the pollinator species and 4.9% of the interactions). The high turnover in species-to-species interactions was mainly the effect of species turnover (c. 70% in pairwise comparisons among years), and less the effect of species flexibility to interact with new partners (c. 30%). We conclude that specialization in plant-pollinator interactions might be highly overestimated when measured over short periods of time. This is because many plant or pollinator species appear as specialists in 1 year, but tend to be generalists or to interact with different partner species when observed in other years. The high temporal plasticity in species composition and interaction identity coupled with the low variation in network structure properties (e.g. degree centralization, connectance, nestedness, average distance and network diameter) imply (i) that tight and specialized coevolution might not be as important as previously suggested and (ii) that plant-pollinator interaction networks might be less prone to detrimental effects of disturbance than previously thought. We suggest that this may be due to the opportunistic nature of plant and animal species regarding the available partner resources they depend upon at any particular time.     

Drivers of plant individual-based pollinator visitation network topology in an arid ecosystem

Interactions with pollinators underlie the structure and function of plant communities. Network analysis is a valuable tool for studying plant-pollinator interactions, but these networks are most frequently built by aggregating interactions at the species level. Interactions are between individuals and an advantage of individual-based networks is the ability to integrate inter-individual variation in traits and environmental context within complex ecological networks. We studied the influence of inter-individual variation on pollinator sharing among foundation shrubs and cactus in a desert ecosystem using plant individual-based pollinator visitation networks. We hypothesized that the traits that alter attractiveness of plants to pollinators will also influence an individual plant's role within the visitation network. Foundation plants growing with higher densities of nearby blooming shrubs had higher pollinator visitation rates and had greater access to the conspecific mating pool, suggesting widespread and diffuse pollination facilitation within this community. Further, shrub density influenced the role of betweenness centrality and the effective number of partners (e^H). Floral display size also influenced the effective number of interaction partners but did not directly influence the centrality measures for individual plants or other measures of network structure despite increasing visitation rates. The individual-based visitation networks were significantly modular and module membership was predicted by species identity and pollinator visitation rates. Ecological and individual context mediate the outcome of pollinator-mediated interactions and are fundamental drivers of whole community structure. This study shows that the density of immediate neighbours can influence the overall structure of plant-pollinator interaction networks. Exploring the contribution of intraspecific variation to community interaction networks will improve our understanding of drivers of community-level ecological dynamics.     

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.     

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.     

Plant-Pollinator Coextinctions and the Loss of Plant Functional and Phylogenetic Diversity

Plant-pollinator coextinctions are likely to become more frequent as habitat alteration and climate change continue to threaten pollinators. The consequences of the resulting collapse of plant communities will depend partly on how quickly plant functional and phylogenetic diversity decline following pollinator extinctions. We investigated the functional and phylogenetic consequences of pollinator extinctions by simulating coextinctions in seven plant-pollinator networks coupled with independent data on plant phylogeny and functional traits. Declines in plant functional diversity were slower than expected under a scenario of random extinctions, while phylogenetic diversity often decreased faster than expected by chance. Our results show that plant functional diversity was relatively robust to plant-pollinator coextinctions, despite the underlying rapid loss of evolutionary history. Thus, our study suggests the possibility of uncoupled responses of functional and phylogenetic diversity to species coextinctions, highlighting the importance of considering both dimensions of biodiversity explicitly in ecological studies and when planning for the conservation of species and interactions.     

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.     

Predicting the effect of competition on secondary plant extinctions in plant–pollinator networks

What are the limitations of models that predict the behavior of an ecological community based on a single type of species interaction? Using plant–pollinator network models as an example, we contrast the predicted vulnerability of a community to secondary extinctions under the assumption of purely mutualistic interactions versus mutualistic and competitive interactions. We find that competition among plant species increases the risk of secondary extinctions and extinction cascades. Simulations over a number of different network structures indicate that this effect is stronger in larger networks, more strongly connected networks and networks with higher plant:pollinator ratios. We conclude that efforts to model plant–pollinator communities will systematically over‐estimate community robustness to species loss if plant competition is ignored. However, because the effect of plant competition depends on network architecture, and because characterization of plant competition is work intensive, we suggest that efforts to account for plant competition in plant–pollinator network models should be focused on large, strongly connected networks with high plant:pollinator ratios.     

Does asymmetric specialization differ between mutualistic and trophic networks?

Recently, plant–pollinator networks have been found to be highly structured in a nested pattern in which specialists interact with generalist species. This structure is often assumed to be particular to mutualistic interactions in opposition to the compartmentalized pattern expected for antagonistic networks. We investigated the presence of asymmetric specialization in a data set assembled from the literature of 20 highly resolved plant–insect herbivore networks and compared them with 24 plant–pollinator networks. Our results indicate that these two types of networks differ, but not in the way it is generally assumed. Asymmetric specialization is present in plant–herbivore networks even if it appears less frequently than in plant–pollinator networks. Indeed, mean and median percentages of species showing asymmetric specialisation in herbivory webs are 33% and 14% respectively, compared to 57% and 60% in pollination webs. Furthermore, the amount of asymmetry is linked with species diversity and not to connectance in plant-pollinator networks whereas the opposite pattern is found in plant–herbivore networks. Our results offer promising perspectives for understanding both the mechanisms that structure ecological communities and their impact on community dynamics depending on the type of interaction.     

The role of local species abundance in the evolution of pollinator attraction in flowering plants

We present a population genetic model that incorporates aspects of pollinator efficiency and abundance to examine the effect of the local plant community on the evolution of floral trait specialization. Our model predicts that plant species evolve to be pollinator specialists on the most effective and common pollinators when their abundance is low relative to other plant species in the community (i.e., conspecific pollen is relatively rare) and evolve to be pollinator generalists when they are numerically dominant (i.e., conspecific pollen is abundant). Strong flower constancy also favors generalist floral traits. Furthermore, generalist species are predicted to differentiate when there is a concave trade-off in attracting pollinator species with different floral trait preferences. This result implies that populations that evolve toward a generalist strategy may be more prone to speciation. Ours is the first theoretical model to include local species abundance explicitly, despite the fact that it has been previously identified as an important factor in the evolution of plant specialization. Our results add a layer of ecological complexity to previous models of floral evolution and therefore have the potential to improve our power to predict circumstances under which specialized and generalized plant-pollinator interactions should evolve.     

Linking Plant Specialization to Dependence in Interactions for Seed Set in Pollination Networks

Studies on pollination networks have provided valuable information on the number, frequency, distribution and identity of interactions between plants and pollinators. However, little is still known on the functional effect of these interactions on plant reproductive success. Information on the extent to which plants depend on such interactions will help to make more realistic predictions of the potential impacts of disturbances on plant-pollinator networks. Plant functional dependence on pollinators (all interactions pooled) can be estimated by comparing seed set with and without pollinators (i.e. bagging flowers to exclude them). Our main goal in this study was thus to determine whether plant dependence on current insect interactions is related to plant specialization in a pollination network. We studied two networks from different communities, one in a coastal dune and one in a mountain. For ca. 30% of plant species in each community, we obtained the following specialization measures: (i) linkage level (number of interactions), (ii) diversity of interactions, and (iii) closeness centrality (a measure of how much a species is connected to other plants via shared pollinators). Phylogenetically controlled regression analyses revealed that, for the largest and most diverse coastal community, plants highly dependent on pollinators were the most generalists showing the highest number and diversity of interactions as well as occupying central positions in the network. The mountain community, by contrast, did not show such functional relationship, what might be attributable to their lower flower-resource heterogeneity and diversity of interactions. We conclude that plants with a wide array of pollinator interactions tend to be those that are more strongly dependent upon them for seed production and thus might be those more functionally vulnerable to the loss of network interaction, although these outcomes might be context-dependent.     

Pollinator individual‐based networks reveal the specialized plant–pollinator mutualism in two biodiverse communities

Generalization of pollination systems is widely accepted by ecologists in the studies of plant–pollinator interaction networks at the community level, but the degree of generalization of pollination networks remains largely unknown at the individual pollinator level. Using potential legitimate pollinators that were constantly visiting flowers in two alpine meadow communities, we analyzed the differences in the pollination network structure between the pollinator individual level and species level. The results showed that compared to the pollinator species‐based networks, the linkage density, interaction diversity, interaction evenness, the average plant linkage level, and interaction diversity increased, but connectance, degree of nestedness, the average of pollinator linkage level, and interaction diversity decreased in the pollinator individual‐based networks, indicating that pollinator individuals had a narrower food niche than their counterpart species. Pollination networks at the pollinator individual level were more specialized at the network level (H′₂) and the plant species node level (d′) than at the pollinator species‐level networks, reducing the chance of underestimating levels of specialization in pollination systems. The results emphasize that research into pollinator individual‐based pollination networks will improve our understanding of the pollination networks at the pollinator species level and the coevolution of flowering plants and pollinators.     

Spatial Heterogeneity Regulates Plant-Pollinator Networks across Multiple Landscape Scales

Mutualistic plant-pollinator interactions play a key role in biodiversity conservation and ecosystem functioning. In a community, the combination of these interactions can generate emergent properties, e.g., robustness and resilience to disturbances such as fluctuations in populations and extinctions. Given that these systems are hierarchical and complex, environmental changes must have multiple levels of influence. In addition, changes in habitat quality and in the landscape structure are important threats to plants, pollinators and their interactions. However, despite the importance of these phenomena for the understanding of biological systems, as well as for conservation and management strategies, few studies have empirically evaluated these effects at the network level. Therefore, the objective of this study was to investigate the influence of local conditions and landscape structure at multiple scales on the characteristics of plant-pollinator networks. This study was conducted in agri-natural lands in Chapada Diamantina, Bahia, Brazil. Pollinators were collected in 27 sampling units distributed orthogonally along a gradient of proportion of agriculture and landscape diversity. The Akaike information criterion was used to select models that best fit the metrics for network characteristics, comparing four hypotheses represented by a set of a priori candidate models with specific combinations of the proportion of agriculture, the average shape of the landscape elements, the diversity of the landscape and the structure of local vegetation. The results indicate that a reduction of habitat quality and landscape heterogeneity can cause species loss and decrease of networks nestedness. These structural changes can reduce robustness and resilience of plant-pollinator networks what compromises the reproductive success of plants, the maintenance of biodiversity and the pollination service stability. We also discuss the possible explanations for these relationships and the implications for landscape planning in agricultural areas.     

Plant-pollinator interactions in tropical monsoon forests in Southeast Asia

Forests with different flora and vegetation types harbor different assemblages of flower visitors, and plant-pollinator interactions vary among forests. In monsoon-dominated East and Southeast Asia, there is a characteristic gradient in climate along latitude, creating a broad spectrum of forest types with potentially diverse pollinator communities. To detect a geographical pattern of plant-pollinator interactions, we investigated flowering phenology and pollinator assemblages in the least-studied forest type, i.e., tropical monsoon forest, in the Vientiane plain in Laos. Throughout the 5-year study, we observed 171 plant species blooming and detected flower visitors on 145 species. Flowering occurred throughout the year, although the number of flowering plant species peaked at the end of dry season. The dominant canopy trees, including Dipterocarpaceae, bloomed annually, in contrast to the supra-annual general flowering that occurs in Southeast Asian tropical rain forests. Among the 134 native plant species, 68 were pollinated by hymenopterans and others by lepidopterans, beetles, flies, or diverse insects. Among the observed bees, Xylocopa, megachilids, and honeybees mainly contributed to the pollination of canopy trees, whereas long-tongued Amegilla bees pollinated diverse perennials with long corolla tubes. This is the first community-level study of plant-pollinator interactions in an Asian tropical monsoon forest ecosystem.     

Community structure of pollination webs of Mauritian heathland habitats

Pollination webs have recently deepened our understanding of complex ecosystem functions and the susceptibility of biotic networks to anthropogenic disturbances. Extensive mutualistic networks from tropical species-rich communities, however, are extremely scarce. We present fully quantitative pollination webs of two plant–pollinator communities of natural heathland sites, one of which was in the process of being restored, on the oceanic island of Mauritius. The web interaction data cover a full flowering season from September 2003 to March 2004 and include all flowering plant and their pollinator species. Pollination webs at both sites were dominated by a few super-abundant, disproportionately well-connected species, and many rare and specialised species. The webs differed greatly in size, reflecting higher plant and pollinator species richness and abundance at the restored site. About one fifth of plant species at the smaller community received <3 visits. The main pollinators were insects from diverse taxonomic groups, while the few vertebrate pollinator species were abundant and highly linked. The difference in plant community composition between sites appeared to strongly affect the associated pollinator community and interactions with native plant species. Low visitation rate to introduced plant species suggested little indirect competition for pollinators with native plant species. Overall, our results indicated that the community structure was highly complex in comparison to temperate heathland communities. We discuss the observed differences in plant linkage and pollinator diversity and abundance between the sites with respect to habitat restoration management and its influence on pollination web structure and complexity. For habitat restoration to be successful in the long term, practitioners should aim to maintain structural diversity to support a species-rich and abundant pollinator assemblage which ensures native plant reproduction.     

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.     

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.     

Invasive plant integration into native plant–pollinator networks across Europe

The structure of plant–pollinator networks has been claimed to be resilient to changes in species composition due to the weak degree of dependence among mutualistic partners. However, detailed empirical investigations of the consequences of introducing an alien plant species into mutualistic networks are lacking. We present the first cross-European analysis by using a standardized protocol to assess the degree to which a particular alien plant species (i.e. Carpobrotus affine acinaciformis, Impatiens glandulifera, Opuntia stricta, Rhododendron ponticum and Solanum elaeagnifolium) becomes integrated into existing native plant–pollinator networks, and how this translates to changes in network structure.Alien species were visited by almost half of the pollinator species present, accounting on average for 42 per cent of the visits and 24 per cent of the network interactions. Furthermore, in general, pollinators depended upon alien plants more than on native plants. However, despite the fact that invaded communities received more visits than uninvaded communities, the dominant role of alien species over natives did not translate into overall changes in network connectance, plant linkage level and nestedness. Our results imply that although supergeneralist alien plants can play a central role in the networks, the structure of the networks appears to be very permeable and robust to the introduction of invasive alien species into the network.     

传粉网络的研究进展:网络的结构和动态

植物与传粉者之间相互作用,构成了复杂的传粉网络。近年来,社会网络分析技术的发展使得复杂生态网络的研究成为可能。从群落水平上研究植物与传粉者之间的互惠关系,为理解群落的结构和动态以及花部特征的演化提供了全新的视角。传粉网络的嵌套结构说明自然界的传粉服务存在冗余,而且是相对泛化的物种主导了传粉。在多年或者多季度的传粉网络中,虽然有很高的物种替换率,但是其网络结构仍然保持相对稳定,说明传粉网络对干扰有很强的抗性。尽管有关网络结构和动态的研究逐渐增多,但传粉网络维持的机制仍不清楚。网络结构可以部分由花部特征与传粉者的匹配来解释,也受到系统发生的制约,影响因素还包括群落构建的时间和物种多样性,以及物种在群落中的位置。开展大尺度群落动态的研究,为探索不同时间尺度、不同物种多样性水平上的传粉网络的生态学意义提供了条件。但已有的研究仍存在不足,比如基于访问观察的网络无法准确衡量传粉者的访问效率和植物间的花粉流动,以及结果受到调查精度区域研究不平衡的制约等。目前的研究只深入到传粉者携带花粉构成成分的水平,传粉者访问植物的网络不能代表植物的整个传粉过程。因此,研究应当更多地深入到物种之间关系对有性生殖的切实影响上。