Pollinator-mediated Interactions Research Articles

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 (eH). 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.

Spatial variation in bidirectional pollinator-mediated interactions between two co-flowering species in serpentine plant communities.

Pollinator-mediated competition and facilitation are two important mechanisms mediating co-flowering community assembly. Experimental studies, however, have mostly focused on evaluating outcomes for a single interacting partner at a single location. Studies that evaluate spatial variation in the bidirectional effects between co-flowering species are necessary if we aim to advance our understanding of the processes that mediate species coexistence in diverse co-flowering communities. Here, we examine geographic variation (i.e. at landscape level) in bidirectional pollinator-mediated effects between co-flowering Mimulus guttatus and Delphinium uliginosum. We evaluated effects on pollen transfer dynamics (conspecific and heterospecific pollen deposition) and plant reproductive success. We found evidence of asymmetrical effects (one species is disrupted and the other one is facilitated) but the effects were highly dependent on geographical location. Furthermore, effects on pollen transfer dynamics did not always translate to effects on overall plant reproductive success (i.e. pollen tube growth) highlighting the importance of evaluating effects at multiple stages of the pollination process. Overall, our results provide evidence of a spatial mosaic of pollinator-mediated interactions between co-flowering species and suggest that community assembly processes could result from competition and facilitation acting simultaneously. Our study highlights the importance of experimental studies that evaluate the prevalence of competitive and facilitative interactions in the field, and that expand across a wide geographical context, in order to more fully understand the mechanisms that shape plant communities in nature.

Floral Color Properties of Serpentine Seep Assemblages Depend on Community Size and Species Richness.

Functional traits, particularly those that impact fitness, can shape the ecological and evolutionary relationships among coexisting species of the same trophic level. Thus, examining these traits and properties of their distributions (underdispersion, overdispersion) within communities can provide insights into key ecological interactions (e.g., competition, facilitation) involved in community assembly. For instance, the distribution of floral colors in a community may reflect pollinator-mediated interactions between sympatric plant species, and the phylogenetic distribution of color can inform how evolutionary contingencies can continue to shape extant community assemblages. Additionally, the abundance and species richness of the local habitat may influence the type or strength of ecological interactions among co-occurring species. To evaluate the impact of community size and species richness on mechanisms shaping the distribution of ecologically relevant traits, we examined how floral color (defined by pollinator color vision models) is distributed within co-flowering assemblages. We modeled floral reflectance spectra of 55 co-flowering species using honeybee (Apis mellifera) and syrphid fly (Eristalis tenax) visual systems to assess the distributions of flower color across 14 serpentine seep communities in California. We found that phylogenetic relatedness had little impact on the observed color assemblages. However, smaller seep communities with lower species richness were more overdispersed for flower color than larger, more species-rich communities. Results support that competitive exclusion could be a dominant process shaping the species richness of flower color in smaller-sized communities with lower species richness, but this is less detectable or overwhelmed by other processes at larger, more speciose communities.

Facilitation with a grain of salt: reduced pollinator visitation is an indirect cost of association with the foundation species creosote bush (Larrea tridentata).

In arid ecosystems, shrub facilitation is a critical process driving plant community structure and assembly, often resulting in increased densities of annual plants beneath shrub canopies. Pollinator-mediated interactions can have fitness consequences for both plant interactors but are largely unexplored as an indirect consequence of direct shrub-annual facilitation. We tested the capacity of the geographically widespread creosote bush (Larrea tridentata) to influence pollinator visitation to its annual understory during its phenological shift into spring flowering. We used small video cameras to record pollinator visitation and foraging behavior on potted transplants of a representative flowering annual. We concurrently evaluated L. tridentata's positive role as a foundation plant in this system by measuring the associated plant and arthropod communities and deploying data loggers to measure understory microclimates. Pollinator visitation to the flowering annual desert dandelion, Malacothrix glabrata, was lower when beneath the canopy of L. tridentata, and further declined throughout the study site as L. tridentata entered full bloom. We confirmed the role of L. tridentata as a foundation species in this system through its concurrent, positive effects on annual plant cover (a proxy for biomass), the abundance and richness of the understory arthropod community and its ability to create stable microclimates. Direct and indirect shrub effects on other species function simultaneously to shift net outcomes even within predominantly net positive facilitation complexes.

Pollination interactions reveal direct costs and indirect benefits of plant–plant facilitation for ecosystem engineers

AbstractAimsEcosystem engineers substantially modify the environment via their impact on abiotic conditions and the biota, resulting in facilitation of associated species that would not otherwise grow. Yet, reciprocal effects are poorly understood as studies of plant–plant interactions usually estimate only benefits for associated species, while how another trophic level may mediate direct and indirect feedback effects for ecosystem engineers is hardly considered.MethodsWe ran a field experiment with two ecosystem engineers (Arenaria tetraquetra and Hormathophylla spinosa) blooming either alone or with associated plants to decompose net effects and to test the hypothesis that pollinator-mediated interactions provide benefits that balance costs of facilitation by ecosystem engineers.Important FindingsWe found that net costs of facilitation are accompanied by pollinator-mediated benefits. Despite ecosystem engineers producing fewer flowers per plant, they were visited by more and more diverse pollinators per flower when blooming with associated plants than when blooming alone. Although seed production per plant was higher when ecosystem engineers bloomed alone, fruit set and seed set varied between species. In one case (A. tetraquetra), fruit and seed sets were negatively affected by the presence of associated plants, whereas, in another case (H. spinosa), fruit set and seed set were higher and unaffected when ecosystem engineers bloomed with associated plants, respectively. Our findings suggest that besides experiencing direct costs, ecosystem engineers can also benefit from facilitating other species via increasing their own visibility to pollinators. Thus, we highlight that pollination interactions can compensate for costs of facilitation depending on ecosystem engineer species. This study illuminates how the outcome of direct plant–plant interactions might be mediated by indirect interactions including third players.

Pollinator-mediated interactions between cultivated papaya and co-flowering plant species.

Many modern crop varieties rely on animal pollination to set fruit and seeds. Intensive crop plantations usually do not provide suitable habitats for pollinators so crop yield may depend on the surrounding vegetation to maintain pollination services. However, little is known about the effect of pollinator‐mediated interactions among co‐flowering plants on crop yield or the underlying mechanisms. Plant reproductive success is complex, involving several pre‐ and post‐pollination events; however, the current literature has mainly focused on pre‐pollination events in natural plant communities. We assessed pollinator sharing and the contribution to pollinator diet in a community of wild and cultivated plants that co‐flower with a focal papaya plantation. In addition, we assessed heterospecific pollen transfer to the stigmatic loads of papaya and its effect on fruit and seed production. We found that papaya shared at least one pollinator species with the majority of the co‐flowering plants. Despite this, heterospecific pollen transfer in cultivated papaya was low in open‐pollinated flowers. Hand‐pollination experiments suggest that heterospecific pollen transfer has no negative effect on fruit production or weight, but does reduce seed production. These results suggest that co‐flowering plants offer valuable floral resources to pollinators that are shared with cultivated papaya with little or no cost in terms of heterospecific pollen transfer. Although HP reduced seed production, a reduced number of seeds per se are not negative, given that from an agronomic perspective the number of seeds does not affect the monetary value of the papaya fruit.

No consistent pollinator-mediated impacts of alien plants on natives.

The introduction of an alien plant is widely assumed to have negative consequences for the pollinator-mediated fitness of nearby natives. Indeed, a number of studies, including a highly cited meta-analysis, have concluded that the trend for such interactions is competitive. Here we provide evidence that publication bias and study design have obscured our ability to assess the pollinator-mediated impacts of alien plants. In a meta-analysis of 76 studies, we demonstrate that alien/native status does not predict the outcome of pollinator-mediated interactions among plants. Moreover, we found no evidence that similarity in floral traits or phylogenetic distance between species pairs influences the outcome of pollinator-mediated interactions. Instead, we report that aspects of study design, such as distance between the control and nearest neighbour, and/or the arrangement of study plants better predict the impact of a neighbour than does alien/native status. Our study sheds new light on the role that publication bias and experimental design play in the evaluation of key patterns in ecology. We conclude that, due to the absence of clear, generalisable pollinator-mediated impacts of alien species, management schemes should base decisions on community-wide assessments of the impacts of individual alien plant species, and not solely on alien/native status itself.

Pollinator-mediated interactions in experimental arrays vary with neighbor identity

Premise of the study Local ecological conditions influence the impact of species interactions on evolution and community structure. We investigated whether pollinator-mediated interactions between coflowering plants vary with plant density, coflowering neighbor identity, and flowering season. Methods We conducted a field experiment in which flowering time and floral neighborhood were manipulated in a factorial design. Early- and late-flowering Clarkia unguiculata plants were placed into arrays with C. biloba neighbors, noncongeneric neighbors, additional conspecific plants, or no additional plants as a density control. We compared whole-plant pollen limitation of seed set, pollinator behavior, and pollen deposition among treatments. Key results Interactions mediated by shared pollinators depended on the identity of the neighbor and possibly changed through time, although flowering-season comparisons were compromised by low early-season plant survival. Interactions with conspecific neighbors were likely competitive late in the season. Interactions with C. biloba appeared to involve facilitation or neutral interactions. Interactions with noncongeners were more consistently competitive. The community composition of pollinators varied among treatment combinations. Conclusions Pollinator-mediated interactions involved competition and likely facilitation, depending on coflowering neighbor. Experimental manipulation helped to reveal context-dependent variation in indirect biotic interactions.

Low interspecific pollen transfer between invasive aquatic Ludwigia grandiflora and native co-flowering plants

Showy invasive alien plants are often integrated in the diet of generalist pollinators and because of the lack of co-evolvement with the native plant community, a high amount of interspecific pollen transfer (IPT) can be expected. We investigated pollinator switching and magnitude plus distance of IPT between the alien aquatic Ludwigia grandiflora and the native Lythrum salicaria in both directions in uninvaded and invaded sites with a different relative abundance of L. grandiflora (% cover of the alien plant: no cover; low cover: <5%; high cover: 50–75%). A field experiment was conducted to include both pollinator interspecific movements and tracking of IPT, using fluorescent dye as a pollen analogue. Despite a substantial overlap in pollinators between L. grandiflora and the native L. salicaria, less than 10% of the observed flights were interspecific. Similar results were found in dye transfer patterns. The proportions of stigmas with conspecific dye were always higher than the proportions of stigmas with heterospecific dye for L grandiflora and L. salicaria. There were no differences in conspecific dye loads for L. salicaria between uninvaded and invaded sites. Conspecific pollen loss (native CPL) and heterospecific pollen deposition (alien HPD) were in general low and species-specific. The distance of HPD ranged respectively from 1.7 to 39 m and from 0.3 to 54.8 m in the low cover and high cover sites while CPL ranged respectively from 6.40 to 68.02 m and from 0.60 to 40.18 m in the low cover and high cover sites. We can conclude that, in this system, CPL and HPD will play a minor role in pollinator-mediated interaction. Furthermore, interspecific competition for pollinators will cover a larger distance than just neighboring individuals. Our results suggest the necessity to consider the combined effect of insect visitation, pollen deposition, relative alien abundance, distance and seed set when investigating pollinator-mediated interactions of invasive plants.

Pollinator-mediated interactions in experimental arrays vary with neighbor identity.

Local ecological conditions influence the impact of species interactions on evolution and community structure. We investigated whether pollinator-mediated interactions between coflowering plants vary with plant density, coflowering neighbor identity, and flowering season. We conducted a field experiment in which flowering time and floral neighborhood were manipulated in a factorial design. Early- and late-flowering Clarkia unguiculata plants were placed into arrays with C. biloba neighbors, noncongeneric neighbors, additional conspecific plants, or no additional plants as a density control. We compared whole-plant pollen limitation of seed set, pollinator behavior, and pollen deposition among treatments. Interactions mediated by shared pollinators depended on the identity of the neighbor and possibly changed through time, although flowering-season comparisons were compromised by low early-season plant survival. Interactions with conspecific neighbors were likely competitive late in the season. Interactions with C. biloba appeared to involve facilitation or neutral interactions. Interactions with noncongeners were more consistently competitive. The community composition of pollinators varied among treatment combinations. Pollinator-mediated interactions involved competition and likely facilitation, depending on coflowering neighbor. Experimental manipulation helped to reveal context-dependent variation in indirect biotic interactions.

Evaluating the effects of pollinator-mediated interactions using pollen transfer networks: evidence of widespread facilitation in south Andean plant communities.

Information about the relative importance of competitive or facilitative pollinator-mediated interactions in a multi-species context is limited. We studied interspecific pollen transfer (IPT) networks to evaluate quantity and quality effects of pollinator sharing among plant species on three high-Andean communities at 1600, 1800 and 2000m a.s.l. To estimate the sign of the effects (positive, neutral or negative), the relation between conspecific and heterospecific pollen deposited on stigmas was analysed with GLMMs. Network analyses showed that communities were characterised by the presence of pollen hub-donors and receptors. We inferred that facilitative and neutral pollinator-mediated interactions among plants prevailed over competition. Thus, the benefits from pollinator sharing seem to outweigh the costs (i.e. heterospecific deposition and conspecific pollen loss). The largest proportion of facilitated species was found at the highest elevation community, suggesting that under unfavourable conditions for the pollination service and at lower plant densities facilitation can be more common.

Pollinator-mediated assemblage processes in California wildflowers.

Community assembly is the result of multiple ecological and evolutionary forces that influence species coexistence. For flowering plants, pollinators are often essential for plant reproduction and establishment, and pollinator-mediated interactions may influence plant community composition. Here, we use null models and community phylogenetic analyses of co-occurrence patterns to determine the role of pollinator-mediated processes in structuring plant communities dominated by congeners. We surveyed three species-rich genera (Limnanthes, Mimulus and Clarkia) with centres of diversity in the Sierra Nevada of California. Each genus contains species that co-flower and share pollinators, and each has a robust phylogeny. Within each genus, we surveyed 44-48communities at three spatial scales, measured floral and vegetative traits and tested for segregation or aggregation of: (i) species, (ii) floral traits (which are likely to be influenced by pollinators), and (iii) vegetative traits (which are likely affected by other environmental factors). We detected both aggregation and segregation of floral traits that were uncorrelated with vegetative trait patterns; we infer that pollinators have shaped the community assembly although the mechanisms may be varied (competition, facilitation, or filtering). We also found that mating system differences may play an important role in allowing species co-occurrence. Together, it appears that pollinators influence community assemblage in these three clades.

Asteraceae invaders have limited impacts on the pollination of common native annual species in SW Western Australia’s open woodland wildflower communities

The York gum–jam woodlands of southwest Western Australia support diverse annual wildflower communities despite extensive habitat fragmentation, remnant isolation and the invasion of many exotic annual plant species. Few studies have explored the pollinator–plant relationships maintaining these persistently species-rich ‘novel’ communities. We examine the pollination ecology of five native species common to York gum–jam woodland annual communities to determine whether native pollinators may be mediating impacts of exotic annual plants on native wildflower species. We determined the pollination requirements of native focal species and the diversity and frequency of pollinator visitation to these focal plant species across invasion gradients. We also recorded the pollinator community of a dominant exotic herb in this system: Arctotheca calendula (cape weed). Only two of the five native species examined had significant seed set benefits attributable to insect pollination. One native plant species, Podotheca gnaphalioides, had pollinator assemblages that overlapped significantly with exotic A. calendula, with some reduction in pollinator visitation evident. One species, Waitzia acuminata, was found to benefit from insect pollination only in the larger of two surveyed remnants, which may reflect emerging reproductive polymorphism among geographically isolated populations. We highlight two mechanisms in this system that may buffer pollinator-mediated impacts of exotic species on native species: autonomous seed production, which may be increasingly prevalent in isolated populations, and segregation of pollinator resources among species. Our findings illustrate the ways that pollinator-mediated interactions can affect seed set within plant communities persisting in highly fragmented and invaded agricultural landscapes.

Progress in pollination ecology at the community level

Co-flowering plant species may share pollinators within a community, while pollinators may collect rewards from different plant species, stimulating studies of pollination ecology at the community level. Studies of the interactions between plants and pollinators and between plant species in communities, as opposed to studying individual plant species, could provide more evidence for pollinator-mediated flower evolution, interspecific competition, and how communities assemble. Plant-pollinator interactions have been incorporated into network constructions to study the influence of dynamic pollination networks on plant reproduction. Studies of pollination networks could provide new insights into the evolution of floral traits, especially in sympatric species within natural communities. Previous studies of pollinator-mediated interactions between plant species have generally focused on two or a few plant species rather than numerous co-flowering species. Recent studies have emphasized factors that affect pollen fate, such as pollination efficiency, pollen interference on stigmas, and pollen loss when a pollinator visits different plant species. The fundamental ecological service of pollination is increasingly affected by anthropogenic forces, especially the negative consequences of biological invasions and habitat fragmentation. These challenges highlight the importance of biodiversity conservation and ecological restoration. Studies of pollination ecology at the community level have recently emerged in China. However, more observational and experimental studies at multiple spatio-temporal scales are required to explore plant-pollinator and plant-plant interactions and to enhance our understanding of community assemblages, species interactions, and floral evolution at a larger scale.

Presence of an invasive plant species alters pollinator visitation to a native

The degree to which pollinator-mediated interactions assist or impede plant invasions is currently poorly understood. Here we describe the findings of an experiment designed to investigate how pollinator-mediated interactions between invasive Lythrum salicaria (Purple loosestrife) and a closely related native North American species, Decodon verticillatus (Swamp loosestrife) are influenced by the stage of invasion (i.e., early or late). By comparing pollinator preference and constancy to plants in experimentally introduced arrays of L. salicaria and D. verticillatus in invaded and uninvaded communi- ties, we were able to simulate the ecological implica- tions of two different stages of L. salicaria invasion. Invasion status had no significant effect on pollinator visitation to L. salicaria and D. verticillatus when all pollinator taxa were considered together. However, when bumblebees, the dominant pollinator at all sites, were considered alone, we found a significant inter- action between pollinator preference and the invasion status of the site, with D. verticillatus preferred at uninvaded sites only, and no preference exhibited at invaded sites. In addition, for all pollinator taxa, we found that interspecific pollinator movements were overrepresented at uninvaded sites and underrepre- sented at invaded sites, suggesting that heterospecific pollen deposition could be a significant impediment to pollinator-mediated reproduction for both species in the early stages of an invasion. We discuss the potential consequences of our findings to the estab- lishment of animal-pollinated invasive plants and the persistence of native species in the face of invasion.

The effect of invasiveLythrum salicariapollen deposition on seed set in the native speciesDecodon verticillatus

Relatively little attention has been paid to pollinator-mediated interactions among invasive and native plants in spite of the fact that pollen transfer between species in invaded communities has been shown to occur. In this study, we investigated the impact of pollen deposition from the invasive plant species Lythrum salicaria on seed set in a native species that is a member of the same family, Decodon verticillatus. Whole plants were subjected to hand pollination by conspecific (D. verticillatus only) or mixed (a 1:1 mixture of D. verticillatus and L. salicaria) pollen to determine if the addition of a mixed pollen load interferes with the ability of D. verticillatus pollen to set seed. We found the mixed pollen treatment reduced D. verticillatus seed set by 33.3% relative to the conspecific pollen treatment. Our study demonstrates that invasive plants have the potential to negatively impact the reproductive success of a native species through pollinator-mediated interactions. We discuss the potential implications of our findings to the evolution and persistence of native plant populations in invaded communities.

Plant–pollinator interactions between an invasive and native plant vary between sites with different flowering phenology

Floral displays of invasive plants have positive and negative impacts on native plant pollination. Invasive plants may also decrease irradiance, which can lead to reduced pollination of native plants. The effects of shade and flowers of invasive plant species on native plant pollination will depend on overlap in flowering phenologies. We examined the effect of the invasive shrub Lonicera maackii on female reproductive success of the native herb Hydrophyllum macrophyllum at two sites: one with asynchronous flowering phenologies (slight overlap) and one with synchronous (complete overlap). At each site, we measured light availability, pollinator visitation, pollen deposition, and seed set of potted H. macrophyllum in the presence and absence of L. maackii. At both sites, understory light levels were lower in plots containing L. maackii. At the asynchronous site, H. macrophyllum received fewer pollinator visits in the presence of L. maackii, suggesting shade from L. maackii reduced visitation to H. macrophyllum. Despite reduced visitation, H. macrophyllum seed set did not differ between treatments. At the synchronous site, H. macrophyllum received more pollinator visits and produced more seeds per flower in the presence of co-flowering L. maackii compared to plots in which L. maackii was absent, and conspecific pollen deposition was positively associated with seed set. Our results support the hypothesis that co-flowering L. maackii shrubs facilitated pollination of H. macrophyllum, thereby mitigating the negative impacts of shade, leading to increased seed production. Phenological overlap appears to influence pollinator-mediated interactions between invasive and native plants and may alter the direction of impact of L. maackii on native plant pollination.

Plant–pollinator interactions and the assembly of plant communities

Most studies of plant community assembly have focused on how the abiotic aspects of a habitat (e.g. soil moisture or mineral composition) or direct interactions among plants in a community (e.g. competition for space or nutrients) influence which species establish and persist, but they have tended to neglect indirect interactions such as those mediated by pollinators. We address three types of plant-pollinator interactions--filtering, facilitation and competitive exclusion--and their predicted impacts on communities. The few available studies that address how pollinator-mediated interactions limit or promote plant species establishment and persistence provide support for many of these predictions. An integrated framework for understanding plant community assembly needs to incorporate abiotic and biotic interactions, including plant-pollinator and other plant-animal interactions.

POLLINATOR-MEDIATED COMPETITION, REPRODUCTIVE CHARACTER DISPLACEMENT, AND THE EVOLUTION OF SELFING IN ARENARIA UNIFLORA (CARYOPHYLLACEAE).

Ecological factors that reduce the effectiveness of cross-pollination are likely to play a role in the frequent evolution of routine self-fertilization in flowering plants. However, we lack empirical evidence linking the reproductive assurance value of selfing in poor pollination environments to evolutionary shifts in mating system. Here, we investigated the adaptive significance of prior selfing in the polymorphic annual plant Arenaria uniflora (Caryophyllaceae), in which selfer populations occur only in areas of range overlap with congener A. glabra. To examine the hypothesis that secondary contact between the two species contributed to the evolution and maintenance of selfing, we used field competition experiments and controlled hand-pollinations to measure the female fitness consequences of pollinator-mediated interspecific interactions. Uniformly high fruit set by selfers in the naturally pollinated field arrays confirmed the reproductive assurance value of selfing, whereas substantial reductions in outcrosser fruit set (15%) and total seed production (20-35%) in the presence of A. glabra demonstrated that pollinator-mediated interactions can provide strong selection for self-pollination. Heterospecific pollen transfer, rather than competition for pollinator service, appears to be the primary mechanism of pollinator-mediated competition in Arenaria. Premating barriers to hybridization between outcrossers and A. glabra are extremely weak. The production of a few inviable hybrid seeds after heterospecific pollination and intermediate seed set after mixed pollinations indicates that A. glabra pollen can usurp A. uniflora ovules. Thus, any visit to A. uniflora by shared pollinators carries a potential female fitness cost. Moreover, patterns of fruit set and seed set in the competition arrays relative to controls were consistent with the receipt of mixed pollen loads, rather than a lack of pollinator visits. Competition through pollen transfer favors preemptive self-pollination and may be responsible for the evolution of a highly reduced floral morphology in A. uniflora selfers as well as their current geographical distribution.