Phenological patterns and pollination network structure in a Venezuelan páramo: a community-scale perspective on plant-animal interactions

ABSTRACT

Background: Little information is available about life history of páramo plants such as phenology and plant-animal interactions.

Aims: We analysed phenological patterns of flowering and characterised the structure of a plant-pollinator network in a Venezuelan páramo in order to identify key species in this ecosystem.

Methods: We counted the number of individuals with flowers of 76 native plant species and recorded their pollinators in 16 permanent plots between 3000 and 4200 m monthly for three years. We used this dataset to develop a plant-pollinator network, on which nine different metrics related to structural properties were calculated.

Results: The flowering of most species concentrated during the rainy season (between May and November), however some species have continuous flowering. The guild of floral visitors included hummingbirds, flower piercers, bumblebees, Diptera and Lepidoptera. The plant – flower visitor interaction network did not exhibit nestedness, but showed a significant specialization index (H2) and high values of functional complementarity.

Conclusions: Páramo plants have the capacity of maintaining a resident nectarivorus fauna (bumblebees and hummingbirds) because of continuous flower offer during the year. However, the plant – pollinator network identified could be very sensitive to the loss component species, owing to high levels of specialisation and functional complementarity.     

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.     

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.     

Factors related to the inter‐annual variation in plants' pollination generalization levels within a community

The number of pollinators of a plant species is considered a measure of its ecological generalization and may have important evolutionary and ecological implications. Many pollination studies report inter‐annual fluctuations in the composition of pollinators to particular species. However, the factors causing such variation are still poorly understood. Here we investigate how flowering duration and plant and pollinator assemblages influenced the inter‐annual changes in the functional generalization level of the 20 most common plant species of a semi‐natural meadow in southern Norway. We also studied the extent to which changes in generalization levels were controlled by flower‐shape and flowering time. Large inter‐annual changes in generalization levels were common and there was no relationship between the generalization level one year and the following. Generalization level of particular plant species increased with flowering duration, sampling effort, and the abundance of managed honeybees in the community. Generalization level decreased with the flowering synchrony between the focal plant species and the rest of the plant community and with the focal species’ own abundance, which we attribute to inter‐specific competition for pollinator attraction and foraging decisions made by pollinators. Plants with different flower‐shapes and flowering times did not differ in the extent of inter‐annual variation in generalization levels. Most studies do not consider the effect of the plant community on the generalization level of particular plant species. We show here that both pollinator and plant assemblages can affect the inter‐annual variation in generalization levels of plant species. Studies like ours will help to understand how pollination interactions are structured at the community level, and the ecological and evolutionary consequences that these inter‐annual changes in generalization levels may have.     

The temporal dimension in individual‐based plant pollination networks

The pollination success of animal‐pollinated plants depends on the temporal coupling between flowering schedules and pollinator availability. Within a population, individual plants exhibiting disparate flowering schedules will be exposed to different pollinators when the latter exhibit temporal turnover. The temporal overlap between individual plants and pollinators will result in a turnover of interactions, which can be analyzed through a network approach. We have explored the temporal dynamics of individual‐based plant networks resulting from pairwise similarities in pollinator composition. During two flowering seasons, we surveyed the phenology and pollinator fauna of the individual plants from a population of Erysimum mediohispanicum (Brassicaceae). We analyzed the topology of these networks by means of their modularity, clustering, and core–periphery structure. These metrics are related to network functional properties such as cohesion, transitivity and centralization respectively. Afterwards, we analyzed the influence of each pollinator functional group on network topology. We found that network topology varied widely over time as a consequence of the differences in plant phenology and the idiosyncratic and contextual effect of pollinators. When integrating all temporary networks, the network became cohesive (non modular), transitive (locally clusterized), and centralized (core–periphery topology). These topologies could entail important consequences for plant reproduction. Our results highlight the importance of considering the entire flowering season and the necessity of making comprehensive temporal sampling when trying to build reliable interaction networks.     

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.     

Comparing two methods for estimating floral resource availability for insect pollinators in semi-natural habitats

Pollinator and flowering plant interactions play a critical role in maintaining most terrestrial ecosystems, including agroecosystems. Although estimates of floral resource availability are essential to understand plant–pollinator relationships, no generally accepted methodology exists to date. We compared two methods for sampling floral resources in a single meadow. About every three days, we recorded species lists of insect-pollinated plants with abundance categories assigned to each species (hereafter referred to as scanning) and we counted the flowering shoots in 36 2 × 2 m quadrats (hereafter quadrat sampling). These methods were compared with respect to (i) the number of species detected, (ii) estimated floral resource abundance, and (iii) temporal changes in flowering. With scanning, we found more potential nectar-plant species and species were found earlier than with quadrat sampling. With the latter, abundant species were found with higher probability than the scarce. Flower abundances were correlated between the two methods. We predicted that a cover of 6.3 ± 3.6% should be used for an appropriate estimate of flower abundance in our study site, although the optimal cover probably varies across different habitats. Furthermore, flower abundance changed 6% per day compared to the flowering peak. Overall, scanning seems to be more appropriate for detecting presence and the timing of species, while quadrats may provide higher resolution for abundance estimates. Increased sampling coverage and frequency may enhance research accuracy and using scanning and quadrat sampling simultaneously may help to optimize research effort. We encourage further development of sampling protocols.     

The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects

Plants are faced with a trade-off between on the one hand growth, development and reproduction and on the other hand defence against environmental stresses. Yet, research on insect-plant interactions has addressed plant-pollinator interactions and plant-attacker interactions separately. Plants have evolved a high diversity of constitutive and induced responses to attack, including the systemic emission of herbivore-induced plant volatiles (HIPVs). The effect of HIPVs on the behaviour of carnivorous insects has received ample attention for leaf-feeding (folivorous) species and their parasitoids and predators. Here, we review whether and to what extent HIPVs affect the interaction of plants in the flowering stage with mutualistic and antagonistic insects. Whereas the role of flower volatiles in the interactions between plants and insect pollinators has received increased attention over the last decade, studies addressing both HIPVs and pollinator behaviour are rare, despite the fact that in a number of plant species herbivory is known to affect flower traits, including size, nectar secretion and composition. In addition, folivory and florivory can also result in significant changes in flower volatile emission and in most systems investigated, pollinator visitation decreased, although exceptions have been found. Negative effects of HIPVs on pollinator visitation rates likely exert negative selection pressure on HIPV emission. The systemic nature of herbivore-induced plant responses and the behavioural responses of antagonistic and mutualistic insects, requires the study of volatile emission of entire plants in the flowering stage. We conclude that approaches to integrate the study of plant defences and pollination are essential to advance plant biology, in particular in the context of the trade-off between defence and growth/reproduction.     

Effects of experimental shifts in flowering phenology on plant-pollinator interactions

Climate change has led to phenological shifts in flowering plants and insect pollinators, causing concern that these shifts will disrupt plant-pollinator mutualisms. We experimentally investigated how shifts in flowering onset affect pollinator visitation for 14 native perennial plant species, six of which have exhibited shifts to earlier flowering over the last 70 years and eight of which have not. We manipulated flowering onset in greenhouses and then observed pollinator visitation in the field. Five of six species with historically advanced flowering received more visits when flowering was experimentally advanced, whereas seven of eight species with historically unchanged flowering received fewer visits when flowering earlier. This pattern suggests that species unconstrained by pollinators have advanced their flowering, whereas species constrained by pollinators have not. In contrast to current concern about phenological mismatches disrupting plant-pollinator mutualisms, mismatches at the onset of flowering are not occurring for most of our study species.     

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.     

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.     

Increasing land-use intensity decreases floral colour diversity of plant communities in temperate grasslands

To preserve biodiversity and ecosystem functions in a globally changing world it is crucial to understand the effect of land use on ecosystem processes such as pollination. Floral colouration is known to be central in plant-pollinator interactions. To date, it is still unknown whether land use affects the colouration of flowering plant communities. To assess the effect of land use on the diversity and composition of flower colours in temperate grasslands, we collected data on the number of flowering plant species, blossom cover and flower reflectance spectra from 69 plant communities in two German regions, Schwäbische Alb (SA) and Hainich-Dün (HD). We analysed reflectance data of flower colours as they are perceived by honeybees and studied floral colour diversity based upon spectral loci of each flowering plant species in the Maxwell triangle. Before the first mowing, flower colour diversity decreased with increasing land-use intensity in SA, accompanied by a shift of mean flower colours of communities towards an increasing proportion of white blossom cover in both regions. By changing colour characteristics of grasslands, we suggest that increasing land-use intensity can affect the flower visitor fauna in terms of visitor behaviour and diversity. These changes may in turn influence plant reproduction in grassland plant communities. Our results indicate that land use is likely to affect communication processes between plants and flower visitors by altering flower colour traits.     

Non-apoid flower-visiting fauna of Everglades National Park, Florida

The non-apoid flower-visiting fauna of Everglades National Park (ENP), Florida, was surveyed during 1995–1997 as part of a community pollinator survey. One hundred and thirty one sampling trips were made to four areas of Everglades National Park (Shark Valley, Chekika, Long Pine Key (LPK), and Flamingo). Species–month curves indicate that the sampling effort resulted in capture of most of the flower-visiting animal species in the park. A total of 143 insects and 1 bird species were recorded. Diptera were the most diverse group (55 spp.), followed by Lepidoptera (42 spp.) and non-apoid Hymenoptera (34 spp.). The majority of species were rare (56% of species were found on fewer than five trips). The highest diversity of species was found from January to May during the peak flowering period in some plant communities. The greatest total diversity was found in Long Pine Key and Shark Valley had the lowest diversity. Chekika and Flamingo were intermediate in diversity. Animals visited 178 plant species,26% of the potentially animal pollinated Angiosperm diversity of the park. Twenty-five species of plants had only non-apoid flower visitors; the majority of these species had only visits by Lepidoptera. Potentially important pollinator species include members of the Syrphidae, Coleoptera, and Lepidoptera. However, many of the flower-visiting species may not be effective pollinators. This study will be useful for designing sampling protocols for including invertebrates in assessments of ecological restoration underway in the Everglades ecosystem and for more detailed studies of the importance of non-apoid flower-visitors as effective pollinators.     

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.     

Floral plasticity: Herbivore‐species‐specific‐induced changes in flower traits with contrasting effects on pollinator visitation

Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant–pollinator interactions. Current knowledge on the full extent of herbivore‐induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore‐induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species‐specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant‐mediated interactions with mutualists.     

Effects of different types of low‐intensity management on plant‐pollinator interactions in Estonian grasslands

In the face of global pollinator decline, extensively managed grasslands play an important role in supporting stable pollinator communities. However, different types of extensive management may promote particular plant species and thus particular functional traits. As the functional traits of flowering plant species (e.g., flower size and shape) in a habitat help determine the identity and frequency of pollinator visitors, they can also influence the structures of plant−pollinator interaction networks (i.e., pollination networks). The aim of this study was to examine how the type of low‐intensity traditional management influences plant and pollinator composition, the structure of plant−pollinator interactions, and their mediation by floral and insect functional traits. Specifically, we compared mown wooded meadows to grazed alvar pastures in western Estonia. We found that both management types fostered equal diversity of plants and pollinators, and overlapping, though still distinct, plant and pollinator compositions. Wooded meadow pollination networks had significantly higher connectance and specialization, while alvar pasture networks achieved higher interaction diversity at a standardized sampling of interactions. Pollinators with small body sizes and short proboscis lengths were more specialized in their preference for particular plant species and the specialization of individual pollinators was higher in alvar pastures than in wooded meadows. All in all, the two management types promoted diverse plant and pollinator communities, which enabled the development of equally even and nested pollination networks. The same generalist plant and pollinator species were important for the pollination networks of both wooded meadows and alvar pastures; however, they were complemented by management‐specific species, which accounted for differences in network structure. Therefore, the implementation of both management types in the same landscape helps to maintain high species and interaction diversity.     

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.     

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.     

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.