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.

Pollen transport networks reveal highly diverse and temporally stable plant-pollinator interactions in an Appalachian floral community.

Floral visitation alone has been typically used to characterize plant-pollinator interaction networks even though it ignores differences in the quality of floral visits (e.g. transport of pollen) and thus may overestimate the number and functional importance of pollinating interactions. However, how network structural properties differ between floral visitation and pollen transport networks is not well understood. Furthermore, the strength and frequency of plant-pollinator interactions may vary across fine temporal scales (within a single season) further limiting our predictive understanding of the drivers and consequences of plant-pollinator network structure. Thus, evaluating the structure of pollen transport networks and how they change within a flowering season may help increase our predictive understanding of the ecological consequences of plant-pollinator network structure. Here we compare plant-pollinator network structure using floral visitation and pollen transport data and evaluate within-season variation in pollen transport network structure in a diverse plant-pollinator community. Our results show that pollen transport networks provide a more accurate representation of the diversity of plant-pollinator interactions in a community but that floral visitation and pollen transport networks do not differ in overall network structure. Pollen transport network structure was relatively stable throughout the flowering season despite changes in plant and pollinator species composition. Overall, our study highlights the need to improve our understanding of the drivers of plant-pollinator network structure in order to more fully understand the process that govern the assembly of these interactions in nature.

Widespread vulnerability of flowering plant seed production to pollinator declines.

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Pollinators contribute to the maintenance of flowering plant diversity.

Mechanisms that favour rare species are key to the maintenance of diverse communities1-3. One of the most critical tasks for conservation of flowering plant biodiversity is to understand how plant-pollinator interactions contribute to the maintenance of rare species4-7. Here we show that niche partitioning in pollinator use and asymmetric facilitation confer fitness advantage of rarer species in a biodiversity hotspot using phylogenetic structural equation modelling that integrates plant-pollinator and interspecific pollen transfer networks with floral functional traits. Co-flowering species filtered pollinators via floral traits, and rarer species showed greater pollinator specialization leading to higher pollination-mediated male and female fitness than more abundant species. When plants shared pollinator resources, asymmetric facilitation via pollen transport dynamics benefitted the rarer species at the cost of more abundant species, serving as an alternative diversity-promoting mechanism. Our results emphasize the importance of community-wide plant-pollinator interactions that affect reproduction for biodiversity maintenance.

Spatial variation in the intensity of interactions via heterospecific pollen transfer may contribute to local and global patterns of plant diversity.

BACKGROUND: Studies that aim to understand the processes that generate and organize plant diversity in nature have a long history in ecology. Among these, the study of plant-plant interactions that take place indirectly via pollinator choice and floral visitation has been paramount. Current evidence, however, indicates that plants can interact more directly via heterospecific pollen (HP) transfer and that these interactions are ubiquitous and can have strong fitness effects. The intensity of HP interactions can also vary spatially, with important implications for floral evolution and community assembly. SCOPE: Interest in understanding the role of heterospecific pollen transfer in the diversification and organization of plant communities is rapidly rising. The existence of spatial variation in the intensity of species interactions and their role in shaping patterns of diversity is also well recognized. However, after 40 years of research, the importance of spatial variation in HP transfer intensity and effects remains poorly known, and thus we have ignored its potential in shaping patterns of diversity at local and global scales. Here, I develop a conceptual framework and summarize existing evidence for the ecological and evolutionary consequences of spatial variation in HP transfer interactions and outline future directions in this field. CONCLUSIONS: The drivers of variation in HP transfer discussed here illustrate the high potential for geographic variation in HP intensity and its effects, as well as in the evolutionary responses to HP receipt. So far, the study of pollinator-mediated plant-plant interactions has been almost entirely dominated by studies of pre-pollination interactions even though their outcomes can be influenced by plant-plant interactions that take place on the stigma. It is hence critical that we fully evaluate the consequences and context-dependency of HP transfer interactions in order to gain a more complete understanding of the role that plant-pollinator interactions play in generating and organizing plant biodiversity.

Diversity and composition of pollen loads carried by pollinators are primarily driven by insect traits, not floral community characteristics.

Flowering plants require conspecific pollen to reproduce but they often also receive heterospecific pollen, suggesting that pollinators carry mixed pollen loads. However, little is known about drivers of abundance, diversity or composition of pollen carried by pollinators. Are insect-carried pollen loads shaped by pollinator traits, or do they reflect available floral resources? We quantified pollen on 251 individual bees and 95 flies in a florally diverse community. We scored taxonomic order, sex, body size, hairiness and ecological specialization of pollinators, and recorded composition of available flowers. We used phylogenetically controlled model selection to compare relative influences of pollinator traits and floral resources on abundance, diversity and composition of insect-carried pollen. We tested congruence between composition of pollen loads and available flowers. Pollinator size, specialization and type (female bee, male bee, or fly) described pollen abundance, diversity and composition better than floral diversity. Pollen loads varied widely among insects (10-80,000,000 grains, 1-16 species). Pollen loads of male bees were smaller, but vastly more diverse than those of female bees, and equivalent in size but modestly more diverse than those of flies. Pollen load size and diversity were positively correlated with body size but negatively correlated with insect ecological specialization. These traits also drove variation in taxonomic and phylogenetic composition of insect-carried pollen loads, but composition was only weakly congruent with available floral resources. Qualities of pollinators best predict abundance and diversity of carried pollen indicating that functional composition of pollinator communities may be important to structuring heterospecific pollen transfer among plants.

Impacts of plant invasions in native plant-pollinator networks.

The disruption of mutualisms by invasive species has consequences for biodiversity loss and ecosystem function. Although invasive plant effects on the pollination of individual native species has been the subject of much study, their impacts on entire plant-pollinator communities are less understood. Community-level studies on plant invasion have mainly focused on two fronts: understanding the mechanisms that mediate their integration; and their effects on plant-pollinator network structure. Here we briefly review current knowledge and propose a more unified framework for evaluating invasive species integration and their effects on plant-pollinator communities. We further outline gaps in our understanding and propose ways to advance knowledge in this field. Specifically, modeling approaches have so far yielded important predictions regarding the outcome and drivers of invasive species effects on plant communities. However, experimental studies that test these predictions in the field are lacking. We further emphasize the need to understand the link between invasive plant effects on pollination network structure and their consequences for native plant population dynamics (population growth). Integrating demographic studies with those on pollination networks is thus key in order to achieve a more predictive understanding of pollinator-mediated effects of invasive species on the persistence of native plant biodiversity.

Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.

Plant-pollinator network structural properties differentially affect pollen transfer dynamics and pollination success.

Plant-pollinator network studies have uncovered important generalities in the structure of these communities, rapidly advancing our understanding of the underlying drivers of such a structure. In spite of this, however, it is still unclear how changes in structural network properties influence overall plant pollination success. One key limitation is the lack of information on the relationship between network structural properties and aspects of pollination and plant reproductive success. Here, we estimate four plant species network structural metrics (interaction strength, weighted degree, closeness centrality, and specialization level), commonly used to describe their importance within plant-pollinator networks, at two different sites, and evaluate their effects on pollen deposition and pollen tube success. We found a positive effect of plant-pollinator specialization and a negative effect of closeness centrality on heterospecific pollen load size. We also found a marginal negative effect of closeness centrality on pollen tube success. Our results suggest that increasing plant-pollinator specialization within nested communities (pollinated by one or very few generalist insect species) may result in high levels of heterospecific pollen transfer. Furthermore, the differential effects of plant-pollinator network metrics on pollination success (pollen receipt and pollen tube success), highlight the need to integrate quantity (e.g. visitation rate) and quality (e.g. pollen delivery) aspects of pollination to achieve a more mechanistic understanding of the relationship between plant-pollinator network structure and function. Such knowledge is key to evaluate the resilience and stability of plant-pollinator communities and the services they provide in the face of increasing human disturbances.

Pollen on stigmas as proxies of pollinator competition and facilitation: complexities, caveats and future directions.

BACKGROUND: Pollen transfer via animals is necessary for reproduction by ~80 % of flowering plants, and most of these plants live in multispecies communities where they can share pollinators. While diffuse plant-pollinator interactions are increasingly recognized as the rule rather than the exception, their fitness consequences cannot be deduced from flower visitation alone, so other proxies, functionally closer to seed production and amenable for use in a broad variety of diverse communities, are necessary. SCOPE: We conceptually summarize how the study of pollen on stigmas of spent flowers can reflect key drivers and functional aspects of the plant-pollinator interaction (e.g. competition, facilitation or commensalism). We critically evaluate how variable visitation rates and other factors (pollinator pool and floral avoidance) can give rise to different relationships between heterospecific pollen and (1) conspecific pollen on the stigma and (2) conspecific tubes/grain in the style, revealing the complexity of potential interpretations. We advise on best practices for using these proxies, noting the assumptions and caveats involved in their use, and explicate what additional data are required to verify interpretation of given patterns. CONCLUSIONS: We conclude that characterizing pollen on stigmas of spent flowers provides an attainable indirect measure of pollination interactions, but given the complex processes of pollen transfer that generate patterns of conspecific-heterospecific pollen on stigmas these cannot alone determine whether competition or facilitation are the underlying drivers. Thus, functional tests are also needed to validate these hypotheses.

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.

The role of alien species on plant-floral visitor network structure in invaded communities.

The interactions between pairs of native and alien plants via shared use of pollinators have been widely studied. Community level studies however, are necessary in order to fully understand the factors and mechanisms that facilitate successful plant invasion, but these are still scarce. Specifically, few community level studies have considered how differences in invasion level (alien flower abundance), and degree of floral trait similarity between native and invasive species, mediate effects on native plant-pollinator communities. Here, we evaluated the role of alien species on overall plant-floral visitor network structure, and on species-level network parameters, across nine invaded coastal communities distributed along 205 km in Yucatán, México that vary in alien species richness and flower abundance. We further assessed the potential the role of alien plant species on plant-floral visitor network structure and robustness via computational simulation of native and invasive plant extinction scenarios. We did not find significant differences between native and alien species in their functional floral phenotypes or in their visitation rate and pollinator community composition in these invaded sites. Variation in the proportion of alien plant species and flower abundance across sites did not influence plant-pollinator network structure. Species-level network parameters (i.e., normalized degree and nestedness contribution) did not differ between native and alien species. Furthermore, our simulation analyses revealed that alien species are functionally equivalent to native species and contribute equally to network structure and robustness. Overall, our results suggest that high levels of floral trait similarity and pollinator use overlap may help facilitate the integration of alien species into native plant-pollinator networks. As a result, alien species may also play a similar role than that of natives in the structure and stability of native plant and pollinator communities in the studied coastal sand dune ecosystem.

Patterns and effects of heterospecific pollen transfer between an invasive and two native plant species: the importance of pollen arrival time to the stigma.

PREMISE: Invasive plant species can integrate into native plant-pollinator communities, but the underlying mechanisms are poorly understood. Competitive interactions between invasive and native plants via heterospecific pollen (HP) and differential invasive HP effects depending on HP arrival time to the stigma may mediate invasion success, but these have been little studied. METHODS: We evaluated patterns and effects of HP receipt on pollen tube growth in two native and one invasive species in the field. We also used hand-pollination experiments to evaluate the effect of invasive HP pollen and its arrival time on native reproductive success. RESULTS: Native species receive smaller and less-diverse HP loads (5-7 species) compared to invasive species (10 species). The load size of HP had a negative effect on the proportion of pollen tubes in both native species but not in the invasive, suggesting higher HP tolerance in the latter. Invasive HP arrival time differentially affected pollen tube success in native species. CONCLUSIONS: Our results highlight the need to study reciprocal HP effects between invasive and native species and the factors that determine differential responses to HP receipt to fully understand the mechanisms facilitating invasive species integration into native plant-pollinator communities.

Global geographic patterns of heterospecific pollen receipt help uncover potential ecological and evolutionary impacts across plant communities worldwide.

Species interactions are known to be key in driving patterns of biodiversity across the globe. Plant-plant interactions through heterospecific pollen (HP) transfer by their shared pollinators is common and has consequences for plant reproductive success and floral evolution, and thus has the potential to influence global patterns of biodiversity and plant community assembly. The literature on HP transfer is growing and it is therefore timely to review patterns and causes of among-species variation in HP receipt at a global scale, thus uncovering its potential contribution to global patterns of biodiversity. Here we analyzed published data on 245 species distributed across five continents to evaluate latitudinal and altitudinal patterns of HP receipt. We further analyzed the role of floral symmetry and evolutionary history in mediating patterns of HP receipt. Latitude and elevation affected the likelihood and intensity of HP receipt indicating that HP transfer increases in species-rich communities and in areas with high abundance of vertebrate pollinators. Floral symmetry and evolutionary history determined HP load size across plant communities worldwide. Overall, our results suggest that HP receipt may have the potential to contribute to global geographic patterns of plant diversity by imposing strong selective pressures in species-rich areas across the globe.

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

Interactive effects between donor and recipient species mediate fitness costs of heterospecific pollen receipt in a co-flowering community.

Evaluation of pollen transfer in wild plant communities revealing heterospecific pollen receipt is common, yet experimental hand pollinations have revealed high among-species variation in the magnitude of its effect on recipient fitness. The causes of this among-species variation are unknown, however, prompting the investigation of underlying factors. Here, we conducted a hand-pollination experiment with ten co-flowering species to determine whether the effects of heterospecific pollen receipt are mediated by the pollen donor or recipient species alone, or whether the effects are determined by the interaction between them. We further assessed species traits potentially mediating interactive effects in heterospecific pollen receipt by evaluating the relationship between heterospecific pollen effect size and three different predictors reflecting a unique combination of pollen donor and recipient characteristics. Our results show, for the first time, that the magnitude of the heterospecific pollen receipt effect is determined by the specific combination of donor and recipient species (i.e., interactive effects). However, we were unable to uncover the specific combination of traits mediating these effects. Overall, our study provides strong evidence that an understanding of heterospecific pollen receipt effects based on recipient or donor characteristics alone may be insufficient. This study is an important step toward an understanding of consequences of heterospecific pollen receipt in co-flowering communities.

Variation in sampling effort affects the observed richness of plant-plant interactions via heterospecific pollen transfer: implications for interpretation of pollen transfer networks.

PREMISE OF THE STUDY: There is growing interest in understanding plant-plant interactions via pollen transfer at the community level. Studies on the structure and spatial variability of pollen transfer networks have been valuable to this understanding. However, there is high variability in the intensity of sampling used to characterize pollen transfer interactions, which could influence network structure. To date, there is no knowledge of how sampling effort influences the richness of pollen on stigmas and thereby transfer interactions observed, nor how this may vary across species and study sites. METHODS: We use rarefaction curves on 16 species to characterize the relationship between sampling effort (number of stigmas analyzed) and the richness of pollen transfer interactions recorded. We further assess variability in this relationship among species, plant community types, and sites within a single plant community. KEY RESULTS: We show high among-species variation in the amount of sampling required to sufficiently characterize interspecific pollen transfer. We further reveal variability in the sampling effort-interaction richness relationship among different plant communities and even for the same species growing in different sites. CONCLUSIONS: The wide heterogeneity in the sampling effort required to accurately characterize pollen transfer interactions observed has the potential to influence the characterization of pollen transfer dynamics. Thus, sampling completeness should be considered in future studies to avoid overestimation of modularity and specialization in pollen transfer networks that may bias the predicted causes and expected consequences of such processes for plant-plant interactions.

Effects of heterospecific pollen from a wind-pollinated and pesticide-treated plant on reproductive success of an insect-pollinated species.

PREMISE OF THE STUDY: Studies on the effects of heterospecific pollen (HP) transfer have been focused mainly on insect-pollinated species, despite evidence of insect visitation to wind-pollinated species and transfer of their pollen onto stigmas of insect-pollinated plants. Thus, the potential consequences of HP transfer from wind-pollinated species remain largely unknown. Furthermore, accumulation of pesticide residues in pollen of wind-pollinated crops has been documented, but its potential effects on wild plant species via HP transfer have not been tested. METHODS: We evaluated the effect of wind-dispersed Zea mays pollen on pollen tube growth of the insect-pollinated Mimulus nudatus via hand pollinations. We further evaluated whether pesticide-contaminated Z. mays pollen has larger effects on M. nudatus pollen success than non-contaminated Z. mays pollen. KEY RESULTS: We found a significant negative effect of Z. mays pollen on M. nudatus pollen tube growth even when deposited in small amounts. However, we did not observe any difference in the magnitude of this effect between pesticide-laden Z. mays pollen and non-contaminated Z. mays pollen. CONCLUSIONS: Our results suggest that wind-pollinated species can have negative effects as HP donors on insect-pollinated recipients. Thus, their role in shaping co-flowering interactions for wind- and insect-pollinated species deserves more attention. Although we did not find evidence that pesticide contamination increased HP effects, we cannot fully rule out the existence of such an effect, because pollen load and thus the pesticide dose applied to stigmas was low. This result should be confirmed using other HP donors and across a range of HP loads, pesticide types, and concentrations.

Patterns of among- and within-species variation in heterospecific pollen receipt: The importance of ecological generalization.

PREMISE OF THE STUDY: Coflowering plants are at risk for receiving pollen from heterospecifics as well as conspecifics, yet evidence shows wide variation in the degree that heterospecific pollen transfer occurs. Evaluation of patterns and correlates of among- and within-species variation in heterospecific pollen (HP) receipt is key to understanding its importance for floral evolution and species coexistence; however, the rarity of deeply sampled multispecies comparisons has precluded such an evaluation. METHODS: We evaluated patterns of among- and within-species variation in HP load size and diversity in 19 species across three distinct plant communities. We assessed the importance of phenotypic specialization (floral phenotype), ecological specialization (contemporary visitor assemblage), and conspecific flower density as determinants of among-species variation. We present hypotheses for different accrual patterns of HP within species based on the evenness and quality of floral visitors and evaluated these by characterizing the relationship between conspecific pollen (CP) and HP receipt. KEY RESULTS: We found that within-species variation in HP receipt was greater than among-species and among-communities variation. Among species, ecological generalization emerged as the strongest driver of variation in HP receipt irrespective of phenotypic specialization. Within-species variation in HP load size and diversity was predicted most often from two CP-HP relationships (linear or exponentially decreasing), suggesting that two distinct types of plant-pollinator interactions prevail. CONCLUSIONS: Our results give important insights into the potential drivers of among- and within-species variation in HP receipt. They also highlight the value of explorations of patterns at the intraspecific level, which can ultimately shed light on plant-pollinator-mediated selection in diverse plant communities.