Pollen-insect interaction meta-networks identify key relationships for conservation in mosaic agricultural landscapes.

Flower visitors use different parts of the landscape through the plants they visit, however these connections vary within and among land uses. Identifying which flower-visiting insects are carrying pollen, and from where in the landscape, can elucidate key pollen-insect interactions and identify the most important sites for maintaining community-level interactions across land uses. We developed a bipartite meta-network, linking pollen-insect interactions with the sites they occur in. We used this to identify which land-use types at the site- and landscape-scale (within 500 m of a site) are most important for conserving pollen-insect interactions. We compared pollen-insect interactions across four different land uses (remnant native forest, avocado orchard, dairy farm, rotational potato crop) within a mosaic agricultural landscape. We sampled insects using flight intercept traps, identified pollen carried on their bodies and quantified distinct pollen-insect interactions that were highly specialized to both natural and modified land uses. We found that sites in crops and dairy farms had higher richness of pollen-insect interactions and higher interaction strength than small forest patches and orchards. Further, many interactions involved pollinator groups such as flies, wasps, and beetles that are often under-represented in pollen-insect network studies, but were often connector species in our networks. These insect groups require greater attention to enable wholistic pollinator community conservation. Pollen samples were dominated by grass (Poaceae) pollen, indicating anemophilous plant species may provide important food resources for pollinators, particularly in modified land uses. Field-scale land use (within 100 m of a site) better predicted pollen-insect interaction richness, uniqueness, and strength than landscape-scale. Thus, management focused at smaller scales may provide more tractable outcomes for conserving or restoring pollen-insect interactions in modified landscapes. For instance, actions aimed at linking high-richness sites with those containing unique (i.e., rare) interactions by enhancing floral corridors along field boundaries and between different land uses may best aid interaction diversity and connectance. The ability to map interactions across sites using a meta-network approach is practical and can inform land-use planning, whereby conservation efforts can be targeted toward areas that host key interactions between plant and pollinator species.

Biological and behavioral responses of European honey bee (Apis mellifera) colonies to perfluorooctane sulfonate exposure.

Bees provide pollination services to managed and wild ecosystems but are threatened globally due to multiple stressors, including exposure to contaminants. Perfluorooctane sulfonate (PFOS) is a widely detected and persistent contaminant that accumulates and biomagnifies in food chains. In this exposure effect study, small whole colonies of Apis mellifera (1000 bees) were exposed to PFOS using a purpose-built cage system over a 4-week period. The PFOS exposure concentrations were provided to bees in sugar syrup at concentrations detected in the environment, ranging from 0 to 1.6 mg L-1 . A range of biological and behavioral responses were monitored. Bee tissue, honey, and fecal matter were analyzed using isotope dilution combined with liquid chromatography-tandem mass spectrometry adapted for bee and honey matrix analysis. Bee mortality increased significantly with PFOS exposure at 0.8 mg L-1  or greater, and brood development ceased entirely at 0.02 mg L-1  or greater. Colony activity, temperament, hive maintenance, and defense were adversely affected in all PFOS exposure treatments compared with the control, even at the lowest PFOS exposure of 0.02 mg L-1 . Perfluorooctane sulfonate was detected in bee tissue with a mean bioaccumulation factor of 0.3, and it was also identified in honey and in feces collected from the hive cages. These findings provide the first evidence that PFOS exposure adversely affects honey bee colonies and may transfer to honey. With PFOS contaminating thousands of sites worldwide, our study has implications for exposed bee populations under natural conditions, pollination services, the honey industry, and human health. Integr Environ Assess Manag 2021;17:673-683. © 2021 SETAC.

Pollen tube growth from multiple pollinator visits more accurately quantifies pollinator performance and plant reproduction.

Pollination services from animals are critical for both crop production and reproduction in wild plant species. Accurately measuring the relative contributions of different animal taxa to pollination service delivery is essential for identifying key pollinators. However, widely used measures of pollinator effectiveness (e.g., single visit pollen deposition) may be inaccurate where plant reproduction is strongly constrained by pollen quality. Here, we test the efficacy of single and multiple pollinator visits for measuring pollinator performance in a model plant species (apple, Malus domestica Borkh) that is strongly limited by pollen quality. We determined pollination success using a suite of measures (pollen deposition, pollen tube growth, fruit and seed set) from single and multiple pollinator visits. We found that pollen deposition from a single pollinator visit seldom resulted in the growth of pollen tubes capable of eliciting ovule fertilisation and never resulted in fruit or seed production. In contrast, multiple pollinator visits frequently initiated the growth of pollen tubes capable of ovule fertilisation and often led to fruit and seed production. Our findings suggest that single visit pollen deposition may provide a poor measure of pollinator performance when linked to reproductive success of plant species that are constrain by pollen quality. Alternatively, pollen tube growth from single and multiple pollinator visits can provide a measure of pollinator performance that is more closely linked to plant reproduction.

Plant species dominance increases pollination complementarity and plant reproductive function.

Worldwide, anthropogenic change is causing biodiversity loss, disrupting many critical ecosystem functions. Most studies investigating the relationship between biodiversity and ecosystem functioning focus on species richness, predominantly within the context of productivity-related functions. Consequently, there is limited understanding of how other biodiversity measures, such as species evenness (the distribution of abundance among species), affect complex multitrophic functions such as pollination. We explore the effect of species evenness on the ecosystem function of pollination using a controlled experiment with selected plants and insects in flight cages. We manipulated the relative abundances of plant and pollinator species, while holding species richness, composition, dominance order, and total abundance constant. Then, we tested how numerical species evenness affected network structure and consequently, seed production, in our artificial communities. Contrary to our expectation, numerical dominance in plant communities increased complementarity in pollinator use (reduced pollinator sharing) among plant species. As predicted by theory, this increased complementarity resulted in higher seed production for the most dominant and rare plant species in our cages. Our results show that in a controlled experimental setting, numerical species evenness can alter important aspects of plant-pollinator networks and plant reproduction, irrespective of species richness, composition, and total abundance. Extending this understanding of how species evenness affects ecosystem functioning to natural systems is crucial as anthropogenic disturbances continue to alter species' abundances, likely disrupting ecosystem functions long before extinctions occur.

Exotic species enhance response diversity to land-use change but modify functional composition.

Two main mechanisms may buffer ecosystem functions despite biodiversity loss. First, multiple species could share similar ecological roles, thus providing functional redundancy. Second, species may respond differently to environmental change (response diversity). However, ecosystem function would be best protected when functionally redundant species also show response diversity. This linkage has not been studied directly, so we investigated whether native and exotic pollinator species with similar traits (functional redundancy) differed in abundance (response diversity) across an agricultural intensification gradient. Exotic pollinator species contributed most positive responses, which partially stabilized overall abundance of the pollinator community. However, although some functionally redundant species exhibited response diversity, this was not consistent across functional groups and aggregate abundances within each functional group were rarely stabilized. This shows functional redundancy and response diversity do not always operate in concert. Hence, despite exotic species becoming increasingly dominant in human-modified systems, they cannot replace the functional composition of native species.

Hairiness: the missing link between pollinators and pollination.

BACKGROUND: Functional traits are the primary biotic component driving organism influence on ecosystem functions; in consequence, traits are widely used in ecological research. However, most animal trait-based studies use easy-to-measure characteristics of species that are at best only weakly associated with functions. Animal-mediated pollination is a key ecosystem function and is likely to be influenced by pollinator traits, but to date no one has identified functional traits that are simple to measure and have good predictive power. METHODS: Here, we show that a simple, easy to measure trait (hairiness) can predict pollinator effectiveness with high accuracy. We used a novel image analysis method to calculate entropy values for insect body surfaces as a measure of hairiness. We evaluated the power of our method for predicting pollinator effectiveness by regressing pollinator hairiness (entropy) against single visit pollen deposition (SVD) and pollen loads on insects. We used linear models and AICC model selection to determine which body regions were the best predictors of SVD and pollen load. RESULTS: We found that hairiness can be used as a robust proxy of SVD. The best models for predicting SVD for the flower species Brassica rapa and Actinidia deliciosa were hairiness on the face and thorax as predictors (R2 = 0.98 and 0.91 respectively). The best model for predicting pollen load for B. rapa was hairiness on the face (R2 = 0.81). DISCUSSION: We suggest that the match between pollinator body region hairiness and plant reproductive structure morphology is a powerful predictor of pollinator effectiveness. We show that pollinator hairiness is strongly linked to pollination-an important ecosystem function, and provide a rigorous and time-efficient method for measuring hairiness. Identifying and accurately measuring key traits that drive ecosystem processes is critical as global change increasingly alters ecological communities, and subsequently, ecosystem functions worldwide.