Predicting plant-pollinator interactions: concepts, methods, and challenges.

Plant-pollinator interactions are ecologically and economically important, and, as a result, their prediction is a crucial theoretical and applied goal for ecologists. Although various analytical methods are available, we still have a limited ability to predict plant-pollinator interactions. The predictive ability of different plant-pollinator interaction models depends on the specific definitions used to conceptualize and quantify species attributes (e.g., morphological traits), sampling effects (e.g., detection probabilities), and data resolution and availability. Progress in the study of plant-pollinator interactions requires conceptual and methodological advances concerning the mechanisms and species attributes governing interactions as well as improved modeling approaches to predict interactions. Current methods to predict plant-pollinator interactions present ample opportunities for improvement and spark new horizons for basic and applied research.

Individual bee foragers are less-efficient transporters of pollen for plants from which they collect the most pollen in their scopae.

PREMISE: Bees provision most of the pollen removed from anthers to their larvae and transport only a small proportion to stigmas, which can negatively affect plant fitness. Though most bee species collect pollen from multiple plant species, we know little about how the efficiency of bees' pollen transport varies among host plant species or how it relates to other aspects of generalist bee foraging behavior that benefit plant fitness, such as specialization on individual foraging bouts. METHODS: We compared the pollen collected and transported by three bee species for 46 co-occurring plant species. Specifically, we compared the relative abundance of pollen taxa in the individual bees' scopae, structures where bees store pollen to provision larvae, with the relative abundance of pollen taxa on the rest of bees' bodies, which is more likely to be transferred to stigmas. RESULTS: Bees carried five times more pollen grains in their scopae than elsewhere on their bodies. Within foraging bouts, bees were relatively specialized in their pollen collection, but transported proportionally less pollen for the host plants on which they specialized. Across foraging bouts, two bee species transported proportionally less pollen for some of their host plants than for others, though differences didn't consistently follow the same trend as at the foraging bout scale. CONCLUSIONS: Our results suggest that foraging-bout specialization, which is known to reduce heterospecific pollen transfer, also results in less-efficient pollen transport. Thus, bee foragers that visit predominantly one plant species may have contrasting effects on that plant's fitness.

Rare and declining bee species are key to consistent pollination of wildflowers and crops across large spatial scales.

Biodiversity promotes ecosystem function (EF) in experiments, but it remains uncertain how biodiversity loss affects function in larger-scale natural ecosystems. In these natural ecosystems, rare and declining species are more likely to be lost, and function needs to be maintained across space and time. Here, we explore the importance of rare and declining bee species to the pollination of three wildflowers and three crops using large-scale (72 sites across 5000 km2 ), multi-year datasets. Half of the sampled bee species (82/164) were rare or declining, but these species provided only ~15% of overall pollination. To determine the number of species important to EF, we used two methods of "scaling up," both of which have previously been used for biodiversity-function analysis. First, we summed bee species' contributions to pollination across space and time and then found the minimum set of species needed to provide a threshold level of function across all sites; according to this method, effectively no rare and declining bee species were important to pollination. Second, we account for the "insurance value" of biodiversity by finding the minimum set of bee species needed to simultaneously provide a threshold level of function at each site in each year. The second method leads to the conclusion that 25 rare and eight declining bee species (36% and 53% of all rare and declining bee species, respectively) are included in the minimum set. Our findings provide some of the strongest evidence yet that rare and declining species are key to meeting threshold levels of EF, thereby providing a more direct link between real-world biodiversity loss and EF.

Greater bee diversity is needed to maintain crop pollination over time.

The current biodiversity crisis underscores the need to understand how biodiversity loss affects ecosystem function in real-world ecosystems. At any one place and time, a few highly abundant species often provide the majority of function, suggesting that function could be maintained with relatively little biodiversity. However, biodiversity may be critical to ecosystem function at longer timescales if different species are needed to provide function at different times. Here we show that the number of wild bee species needed to maintain a threshold level of crop pollination increased steeply with the timescale examined: two to three times as many bee species were needed over a growing season compared to on a single day and twice as many species were needed over six years compared to during a single year. Our results demonstrate the importance of pollinator biodiversity to maintaining pollination services across time and thus to stable agricultural output.

Price Equations for Understanding the Response of Ecosystem Function to Community Change.

AbstractThe relationship between biodiversity and ecosystem function (BEF) remains unclear in many natural ecosystems, partially for lack of theoretical and analytical tools that match common characteristics of observational community data. The ecological Price equation promises to meet this need by organizing many different species-level changes into a few ecologically meaningful categories that sum to total ecosystem function change. Current versions of the ecological Price equation focus on species richness and presence-absence. However, abundance and relative abundance are better estimated in samples and are likely showing a stronger response to global change. Here, we present a novel, abundance-based version of the ecological Price equation in both discrete and continuous forms and explain the similarities and differences between this method and a related, previously developed richness-based method. We also present new empirical techniques for applying the Price equation to ecological data. Our two demonstration analyses reveal how additive effects of increasing abundance on total function are modified by concurrent selection effects due to shifts in species' composition as well as intraspecific change in species' per capita function. The ecological Price equations derived here complement existing approaches and together offer BEF researchers analytical tools and a unifying framework for studying BEF in observational community data.

Many bee species, including rare species, are important for function of entire plant-pollinator networks.

It is important to understand how biodiversity, including that of rare species, affects ecosystem function. Here, we consider this question with regard to pollination. Studies of pollination function have typically focused on pollination of single plant species, or average pollination across plants, and typically find that pollination depends on a few common species. Here, we used data from 11 plant-bee visitation networks in New Jersey, USA, to ask whether the number of functionally important bee species changes as we consider function separately for each plant species in increasingly diverse plant communities. Using rarefaction analysis, we found the number of important bee species increased with the number of plant species. Overall, 2.5 to 7.6 times more bee species were important at the community scale, relative to the average plant species in the same community. This effect did not asymptote in any of our datasets, suggesting that even greater bee biodiversity is needed in real-world systems. Lastly, on average across plant communities, 25% of bee species that were important at the community scale were also numerically rare within their network, making this study one of the strongest empirical demonstrations to date of the functional importance of rare species.

The contribution of plant spatial arrangement to bumble bee flower constancy.

Floral constancy of foraging bees influences plant reproduction. Constancy as observed in nature arises from at least four distinct mechanisms frequently confounded in the literature: context-independent preferences for particular plant species, preferential visitation to the same species as the previous plant visited (simple constancy), the spatial arrangement of plants, and the relative abundances of co-flowering species. To disentangle these mechanisms, we followed individual bee flight paths within patches where all flowering plants were mapped, and we used step selection models to estimate how each mechanism influences the probability of selecting any particular plant given the available plants in a multi-species community. We found that simple constancy was positive: bees preferred to visit the same species sequentially. In addition, bees preferred to travel short distances and maintain their direction of travel between plants. After accounting for distance, we found no significant effect of site-level plant relative abundances on bee foraging choices. To explore the importance of the spatial arrangement of plants for bee foraging choices, we compared our full model containing all parameters to one with spatial arrangement removed. Due to bees' tendency to select nearby plants, combined with strong intraspecific plant clumping, spatial arrangement was responsible for about 50% of the total observed constancy. Our results suggest that floral constancy may be overestimated in studies that do not account for the spatial arrangement of plants, especially in systems with intraspecific plant clumping. Plant spatial patterns at within-site scales are important for pollinator foraging behavior and pollination success.

CropPol: A dynamic, open and global database on crop pollination.

Seventy five percent of the world's food crops benefit from insect pollination. Hence, there has been increased interest in how global change drivers impact this critical ecosystem service. Because standardized data on crop pollination are rarely available, we are limited in our capacity to understand the variation in pollination benefits to crop yield, as well as to anticipate changes in this service, develop predictions, and inform management actions. Here, we present CropPol, a dynamic, open, and global database on crop pollination. It contains measurements recorded from 202 crop studies, covering 3,394 field observations, 2,552 yield measurements (i.e., berry mass, number of fruits, and fruit density [kg/ha], among others), and 47,752 insect records from 48 commercial crops distributed around the globe. CropPol comprises 32 of the 87 leading global crops and commodities that are pollinator dependent. Malus domestica is the most represented crop (32 studies), followed by Brassica napus (22 studies), Vaccinium corymbosum (13 studies), and Citrullus lanatus (12 studies). The most abundant pollinator guilds recorded are honey bees (34.22% counts), bumblebees (19.19%), flies other than Syrphidae and Bombyliidae (13.18%), other wild bees (13.13%), beetles (10.97%), Syrphidae (4.87%), and Bombyliidae (0.05%). Locations comprise 34 countries distributed among Europe (76 studies), North America (60), Latin America and the Caribbean (29), Asia (20), Oceania (10), and Africa (7). Sampling spans three decades and is concentrated on 2001-2005 (21 studies), 2006-2010 (40), 2011-2015 (88), and 2016-2020 (50). This is the most comprehensive open global data set on measurements of crop flower visitors, crop pollinators and pollination to date, and we encourage researchers to add more datasets to this database in the future. This data set is released for non-commercial use only. Credits should be given to this paper (i.e., proper citation), and the products generated with this database should be shared under the same license terms (CC BY-NC-SA).

Seeing through the static: the temporal dimension of plant-animal mutualistic interactions.

Most studies of plant-animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human-driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant-animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.

Specialist foragers in forest bee communities are small, social or emerge early.

Individual pollinators that specialize on one plant species within a foraging bout transfer more conspecific and less heterospecific pollen, positively affecting plant reproduction. However, we know much less about pollinator specialization at the scale of a foraging bout compared to specialization by pollinator species. In this study, we measured the diversity of pollen carried by individual bees foraging in forest plant communities in the mid-Atlantic United States. We found that individuals frequently carried low-diversity pollen loads, suggesting that specialization at the scale of the foraging bout is common. Individuals of solitary bee species carried higher diversity pollen loads than did individuals of social bee species; the latter have been better studied with respect to foraging bout specialization, but account for a small minority of the world's bee species. Bee body size was positively correlated with pollen load diversity, and individuals of polylectic (but not oligolectic) species carried increasingly diverse pollen loads as the season progressed, likely reflecting an increase in the diversity of flowers in bloom. Furthermore, the seasonal increase in pollen load diversity was stronger for bees visiting trees and shrubs than for bees visiting herbaceous plants. Overall, our results showed that both plant and pollinator species' traits as well as community-level patterns of flowering phenology are likely to be important determinants of individual-level interactions in plant-pollinator communities.

Male and female bees show large differences in floral preference.

BACKGROUND: Intraspecific variation in foraging niche can drive food web dynamics and ecosystem processes. In particular, male and female animals can exhibit different, often cascading, impacts on their interaction partners. Despite this, studies of plant-pollinator interaction networks have focused on the partitioning of the floral community between pollinator species, with little attention paid to intraspecific variation in plant preference between male and female bees. We designed a field study to evaluate the strength and prevalence of sexually dimorphic foraging, and particularly resource preferences, in bees. STUDY DESIGN: We observed bees visiting flowers in semi-natural meadows in New Jersey, USA. To detect differences in flower use against a shared background of resource (flower) availability, we maximized the number of interactions observed within narrow spatio-temporal windows. To distinguish observed differences in bee use of flower species, which can reflect abundance patterns and sampling effects, from underlying differences in bee preferences, we analyzed our data with both a permutation-based null model and random effects models. FINDINGS: We found that the diets of male and female bees of the same species were often dissimilar as the diets of different species of bees. Furthermore, we demonstrate differences in preference between male and female bees. We show that intraspecific differences in preference can be robustly identified among hundreds of unique species-species interactions, without precisely quantifying resource availability, and despite high phenological turnover of both bees and plant bloom. Given the large differences in both flower use and preferences between male and female bees, ecological sex differences should be integrated into studies of bee demography, plant pollination, and coevolutionary relationships between flowers and insects.

Correction: The Allometry of Bee Proboscis Length and Its Uses in Ecology.

[This corrects the article DOI: 10.1371/journal.pone.0151482.].

Species turnover promotes the importance of bee diversity for crop pollination at regional scales.

Ecologists have shown through hundreds of experiments that ecological communities with more species produce higher levels of essential ecosystem functions such as biomass production, nutrient cycling, and pollination, but whether this finding holds in nature (that is, in large-scale and unmanipulated systems) is controversial. This knowledge gap is troubling because ecosystem services have been widely adopted as a justification for global biodiversity conservation. Here we show that, to provide crop pollination in natural systems, the number of bee species must increase by at least one order of magnitude compared with that in field experiments. This increase is driven by species turnover and its interaction with functional dominance, mechanisms that emerge only at large scales. Our results show that maintaining ecosystem services in nature requires many species, including relatively rare ones.

Forest bees are replaced in agricultural and urban landscapes by native species with different phenologies and life-history traits.

Anthropogenic landscapes are associated with biodiversity loss and large shifts in species composition and traits. These changes predict the identities of winners and losers of future global change, and also reveal which environmental variables drive a taxon's response to land use change. We explored how the biodiversity of native bee species changes across forested, agricultural, and urban landscapes. We collected bee community data from 36 sites across a 75,000 km2 region, and analyzed bee abundance, species richness, composition, and life-history traits. Season-long bee abundance and richness were not detectably different between natural and anthropogenic landscapes, but community phenologies differed strongly, with an early spring peak followed by decline in forests, and a more extended summer season in agricultural and urban habitats. Bee community composition differed significantly between all three land use types, as did phylogenetic composition. Anthropogenic land use had negative effects on the persistence of several life-history strategies, including early spring flight season and brood parasitism, which may indicate adaptation to conditions in forest habitat. Overall, anthropogenic communities are not diminished subsets of contemporary natural communities. Rather, forest species do not persist in anthropogenic habitats, but are replaced by different native species and phylogenetic lineages preadapted to open habitats. Characterizing compositional and functional differences is crucial for understanding land use as a global change driver across large regional scales.

A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes.

Agricultural intensification is a leading cause of global biodiversity loss, which can reduce the provisioning of ecosystem services in managed ecosystems. Organic farming and plant diversification are farm management schemes that may mitigate potential ecological harm by increasing species richness and boosting related ecosystem services to agroecosystems. What remains unclear is the extent to which farm management schemes affect biodiversity components other than species richness, and whether impacts differ across spatial scales and landscape contexts. Using a global metadataset, we quantified the effects of organic farming and plant diversification on abundance, local diversity (communities within fields), and regional diversity (communities across fields) of arthropod pollinators, predators, herbivores, and detritivores. Both organic farming and higher in-field plant diversity enhanced arthropod abundance, particularly for rare taxa. This resulted in increased richness but decreased evenness. While these responses were stronger at local relative to regional scales, richness and abundance increased at both scales, and richness on farms embedded in complex relative to simple landscapes. Overall, both organic farming and in-field plant diversification exerted the strongest effects on pollinators and predators, suggesting these management schemes can facilitate ecosystem service providers without augmenting herbivore (pest) populations. Our results suggest that organic farming and plant diversification promote diverse arthropod metacommunities that may provide temporal and spatial stability of ecosystem service provisioning. Conserving diverse plant and arthropod communities in farming systems therefore requires sustainable practices that operate both within fields and across landscapes.

The relative importance of pollinator abundance and species richness for the temporal variance of pollination services.

The relationship between biodiversity and the stability of ecosystem function is a fundamental question in community ecology, and hundreds of experiments have shown a positive relationship between species richness and the stability of ecosystem function. However, these experiments have rarely accounted for common ecological patterns, most notably skewed species abundance distributions and non-random extinction risks, making it difficult to know whether experimental results can be scaled up to larger, less manipulated systems. In contrast with the prolific body of experimental research, few studies have examined how species richness affects the stability of ecosystem services at more realistic, landscape scales. The paucity of these studies is due in part to a lack of analytical methods that are suitable for the correlative structure of ecological data. A recently developed method, based on the Price equation from evolutionary biology, helps resolve this knowledge gap by partitioning the effect of biodiversity into three components: richness, composition, and abundance. Here, we build on previous work and present the first derivation of the Price equation suitable for analyzing temporal variance of ecosystem services. We applied our new derivation to understand the temporal variance of crop pollination services in two study systems (watermelon and blueberry) in the mid-Atlantic United States. In both systems, but especially in the watermelon system, the stronger driver of temporal variance of ecosystem services was fluctuations in the abundance of common bee species, which were present at nearly all sites regardless of species richness. In contrast, temporal variance of ecosystem services was less affected by differences in species richness, because lost and gained species were rare. Thus, the findings from our more realistic landscapes differ qualitatively from the findings of biodiversity-stability experiments.

Measuring partner choice in plant-pollinator networks: using null models to separate rewiring and fidelity from chance.

Recent studies of mutualistic networks show that interactions between partners change across years. Both biological mechanisms and chance could drive these patterns, but the relative importance of these factors has not been separated. We established a field experiment consisting of 102 monospecific plots of 17 native plant species, from which we collected 6713 specimens of 52 bee species over four years. We used these data and a null model to determine whether bee species' foraging choices varied more or less over time beyond the variation expected by chance. Thus we provide the first quantitative definition of rewiring and fidelity as these terms are used in the literature on interaction networks. All 52 bee species varied in plant partner choice across years, but for 27 species this variation was indistinguishable from random partner choice. Another 11 species showed rewiring, varying more across years than expected by chance, while 14 species showed fidelity, indicating that they both prefer certain plant species and are consistent in those preferences across years. Our study shows that rewiring and fidelity both exist in mutualist networks, but that once sampling effects have been accounted for, they are less common than has been reported in the ecological literature.

The Allometry of Bee Proboscis Length and Its Uses in Ecology.

Allometric relationships among morphological traits underlie important patterns in ecology. These relationships are often phylogenetically shared; thus quantifying allometric relationships may allow for estimating difficult-to-measure traits across species. One such trait, proboscis length in bees, is assumed to be important in structuring bee communities and plant-pollinator networks. However, it is difficult to measure and thus rarely included in ecological analyses. We measured intertegular distance (as a measure of body size) and proboscis length (glossa and prementum, both individually and combined) of 786 individual bees of 100 species across 5 of the 7 extant bee families (Hymenoptera: Apoidea: Anthophila). Using linear models and model selection, we determined which parameters provided the best estimate of proboscis length. We then used coefficients to estimate the relationship between intertegular distance and proboscis length, while also considering family. Using allometric equations with an estimation for a scaling coefficient between intertegular distance and proboscis length and coefficients for each family, we explain 91% of the variance in species-level means for bee proboscis length among bee species. However, within species, individual-level intertegular distance was a poor predictor of individual proboscis length. To make our findings easy to use, we created an R package that allows estimation of proboscis length for individual bee species by inputting only family and intertegular distance. The R package also calculates foraging distance and body mass based on previously published equations. Thus by considering both taxonomy and intertegular distance we enable accurate estimation of an ecologically and evolutionarily important trait.

Non-bee insects are important contributors to global crop pollination.

Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25-50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.