Spatial and temporal variation in pollinator effectiveness: do unmanaged insects provide consistent pollination services to mass flowering crops?
1. Recent declines in honeybee populations have focused attention on the potential for unmanaged insects to replace them as pollinators of food crops. The capacity of unmanaged pollinators to replace services currently provided by honeybees depends on the spatial and temporal variability of these services, but few quantitative assessments currently exist. 2. We investigated spatial variation in pollinator importance by comparing pollinator efficiency and effectiveness in stigmatic pollen loads, stigmatic contact and visitation rate between honeybees and the seven most abundant unmanaged taxa in 2007. We assessed temporal variability in pollinator visitation using floral visits recorded three times a day over four consecutive years (2005-2008) in 43 'Pak Choi' Brassica rapa ssp. chinensis mass flowering fields in the Canterbury region of New Zealand. Further, we compared the aggregate effect of the unmanaged pollinator assemblage to the managed honeybee. 3. Pak Choi was visited by many insect species that vary in abundance and effectiveness as pollen transfer agents. There was spatial variation in the four measures of pollinator importance. Pollen deposited on stigmas and flower visits per minute were not significantly different comparing the unmanaged assemblage to honeybees, although stigmatic contact and visitor abundance per number of open flowers were greater in honeybees. 4. Unmanaged taxa were frequent visitors to the crop in all 4 years. The pooled services provided by the unmanaged assemblage did not differ within a day and were equal to or greater than those provided by honeybees in 2 of the 4 years. Pollinator importance changed little irrespective of the spatial and temporal variations among taxa. 5. Synthesis and applications. The results of this study suggest that some unmanaged insect taxa are capable of providing consistent pollination services over a 4-year period in a commercial mass flowering crop. As these taxa already contribute substantially to the pollination of food crops, they offer a safety net in the case of sudden collapse of managed honeybee hives. To optimize pollination services, we recommend pollinator-specific farm management practices that consider the needs of both managed and unmanaged pollinator taxa.
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.
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).
Land cover associations of wild bees visiting flowers in apple orchards across three geographic regions of southeast Australia
The conversion of natural vegetation to agriculture is a leading cause of biodiversity decline globally, and can impact negatively on ecosystem services such as pollination. Global meta-analyses find that crop visitation by wild pollinators increases with the amount of natural or semi-natural vegetation in the surrounding landscape. However, these studies typically test the effect of one land cover type, rather than comparing multiple land cover types, and so do not provide information about the land cover arrangements that maximize crop visitation by wild pollinators. We sampled wild bee visitors to apple flowers in 2017 and 2018, and weeds and native plants in apple orchards in 2018, along landscape gradients of native vegetation and non-crop agricultural cover (open grassy areas, grazed or ungrazed) across three widely-separate agricultural regions of southeast Australia. We compared different land cover types as predictors of wild bee visitation to apple orchards, classifying non-crop land cover as: 1) ‘natural vegetation’ (NV), 2) ‘open grassy areas’ (OGA), and 3) ‘natural vegetation plus open grassy areas’ (NVOGA). The dominant flower-visiting wild bees in apple orchards in all regions were soil-nesting species of Halictidae that appear to be capable of exploiting open areas cleared for agriculture; however, even these taxa were rare or absent from orchards in some regions and years. Wild bee visitation to apples was best predicted by OGA in 2017 (positive association), but no land cover type in 2018, while visitation to weeds and native plants increased with both OGA and NV. Comparing different ways of classifying non-crop land cover is important for identifying land management strategies that maximize crop pollination services. However, managing land cover for wild bees may have negligible impacts on apple pollination in southeast Australia where wild bees are often rare in orchards, exhibit between-year variation in land cover associations, and are vastly outnumbered by honeybees (> 90% of visits to apple flowers).
Predicting bee community responses to land-use changes: Effects of geographic and taxonomic biases
Land-use change and intensification threaten bee populations worldwide, imperilling pollination services. Global models are needed to better characterise, project, and mitigate bees' responses to these human impacts. The available data are, however, geographically and taxonomically unrepresentative; most data are from North America and Western Europe, overrepresenting bumblebees and raising concerns that model results may not be generalizable to other regions and taxa. To assess whether the geographic and taxonomic biases of data could undermine effectiveness of models for conservation policy, we have collated from the published literature a global dataset of bee diversity at sites facing land-use change and intensification, and assess whether bee responses to these pressures vary across 11 regions (Western, Northern, Eastern and Southern Europe; North, Central and South America; Australia and New Zealand; South East Asia; Middle and Southern Africa) and between bumblebees and other bees. Our analyses highlight strong regionally-based responses of total abundance, species richness and Simpson's diversity to land use, caused by variation in the sensitivity of species and potentially in the nature of threats. These results suggest that global extrapolation of models based on geographically and taxonomically restricted data may underestimate the true uncertainty, increasing the risk of ecological surprises.
Diurnal effectiveness of pollination by bees and flies in agricultural 'Brassica rapa': implications for ecosystem resilience
Bees are known to provide pollination services to a wide range of crops, yet flies are rarely included in estimates of function. As bees and flies differ markedly in their life history characteristics and resource needs, they may be active and hence provide pollination services at different times of the day. Here, we explore the differences in bee and fly diurnal activity patterns and how this may impact upon pollination services provided to 'Brassica rapa', a mass-flowering crop. We observed pollinators at two-hourly intervals from 6:00 to 20:00 h in twelve fields in New Zealand in 2004-2005. Overall, bees were most active in the middle of the day and were more effective pollinators than flies, driven primarily by the high pollinator efficiency of 'Apis mellifera' and 'Bombus terrestris'. Some fly taxa however, visited flowers early and late in the day when there were few bees. The results of this study demonstrate that fine-scale temporal dynamics and the spatial distribution of crop pollinators may directly affect the quantity of pollination services. The maintenance of biodiversity in agro-ecosystems may therefore be critical to ensure pollinator taxa are available under a range of environmental conditions.
Deconstructing pollinator community effectiveness
Effective pollination is a complex, context-dependent phenomenon determined by both species-level and community-level factors. While pollinator communities are constituted by interacting organisms in a shared environment, these factors are often simplified or overlooked when quantifying species-level pollinator effectiveness alone. Here, we review the recent literature on pollinator effectiveness to identify the pros and cons of existing methods and outline three important areas for future research: plant-pollinator interactions, heterospecific pollen transfer and variation in pollination outcomes. We conclude that pollinator community effectiveness needs to be acknowledged as a key property of pollination effectiveness in order to fully account for the suite of plant, pollinator and environmental factors known to influence different stages of successful pollination.
Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop
1. The honeybee 'Apis mellifera' is currently in decline worldwide because of the combined impacts of Colony Collapse Disorder and the 'Varroa destructor' mite. In order to gain a balanced perspective of the importance of both wild and managed pollination services, it is essential to compare these services directly, a priori, within a cropping landscape. This process will determine the capacity of other flower visitors to act as honeybee replacements. 2. In a highly modified New Zealand agricultural landscape, we compared the pollination services provided by managed honeybees to unmanaged pollinator taxa (including flies) within a 'Brassica rapa var. chinensis' mass flowering crop. 3. We evaluate overall pollinator effectiveness by separating the pollination service into two components: efficiency (i.e. per visit pollen deposition) and visit rate (i.e. pollinator abundance per available flower and the number of flower visits per minute). 4. We observed 31 species attending flowers of 'B. rapa'. In addition to 'A. mellifera', seven insect species visited flowers frequently. These were three other bees ('Lasioglossum sordidum', 'Bombus terrestris' and 'Leioproctus' sp.) and four flies ('Dilophus nigrostigma', 'Melanostoma fasciatum', 'Melangyna novae'-zelandiae and 'Eristalis tenax'). 5. Two bee species, 'Bombus terrestris' and 'Leioproctus' sp. and one fly, 'Eristalis tenax' were as efficient as the honeybee and as effective (in terms of rate of flower visitation). A higher honeybee abundance, however, resulted in it being the more effective pollinator overall. 6. Synthesis and applications. Alternative land management practices that increase the population sizes of unmanaged pollinator taxa to levels resulting in visitation frequencies as high as 'A. mellifera', have the potential to replace services provided by the honeybee. This will require a thorough investigation of each taxon's intrinsic biology and a change in land management practices to ensure year round refuge, feeding, nesting and other resource requirements of pollinator taxa are met.
Adjacent crop type impacts potential pollinator communities and their pollination services in remnants of natural vegetation
Aim: Pollination plays a crucial role in the conservation of many plant species persisting in fragmented, human-dominated landscapes. Pollinators are known to be instrumental in maintaining genetic diversity and metapopulation dynamics for many plant species and are important for providing ecological services that are essential in agricultural landscapes where populations of native plants are highly isolated. Numerous studies have explored the value of remnant native vegetation for supporting pollination services to crop species, yet the effect of mass-flowering crops on the pollinator communities and the pollination services they provide to native plant communities persisting in fragmented landscapes are less well understood. Here, we assess the influence of the presence and phenology of a mass-flowering crop to pollinator community structure, abundance, and pollen load composition in remnant vegetation in complex agricultural landscapes.
Location: South-west Western Australia, Australia.
Methods: We recorded the composition and abundance of insect flower visitors and their pollen loads in isolated remnants of York Gum-Jam woodlands adjacent to canola (insect-attracting) or wheat (non-insect-attracting) fields over two years.
Results: All bees were much more sensitive to adjacent crop type (neighbouring canola or wheat) than non-bee pollinators. Honeybees were the most abundant pollinators in canola fields during peak flowering. Honeybee abundance increased in canola-adjacent reserves post canola bloom, potentially indicating a movement into reserves as crop flowering waned. Native bees were the most diverse in remnant vegetation. Pollen loads of native bees were more mixed (increased pollen richness and evenness) when sampled next to canola fields compared to wheat fields.
Main conclusion: The availability of potential insect pollinators to remnant wildflower communities in agricultural landscapes is context dependent. Whether sampled communities were adjacent to wheat or canola in a landscape significantly impacted the abundance of potential pollinators in certain landscape elements, but not others, and the composition of pollen loads carried by these insects. Results offer novel insights about the influence of landscape context on pollinator communities and the potential pollination services available for the conservation of native plant species in highly fragmented agricultural landscapes.
Pollen transport differs among bees and flies in a human-modified landscape
Aim: Dispersal distances of insect pollinators are critical in defining their contribution to landscape-wide pollen movement and ultimately gene flow in natural and agricultural systems. We ask whether bee and fly pollinator taxa differ in their dispersal distances and transport of viable pollen in a human-modified system. Location: Canterbury and Otago region, South Island, New Zealand. Methods: We captured pollen-carrying insects travelling outside of a model mass-flowering agricultural crop, 'Brassica rapa', using insect flight intercept traps at five distances (0, 100, 200, 300 and 400 m) from the pollen source. We examined pollen loads and pollen viability to determine whether pollen transport distance and viability differ among pollinator taxa. Results: A total of 5453 insects were collected of which 717 individuals from 26 insect taxa were positively identified as dispersing pollen up to 400 m from the source. These taxa consisted of four species from two bee families (Hymenoptera: Apidae and Halictidae), and eight species from four fly families (Diptera: Bibiondae, Stratiomyidae, Syrphidae and Tachinidae). Apidae generally carried higher pollen loads and more viable pollen than most fly taxa. Taxa in the fly families Stratiomyidae and Syrphidae, however, carried pollen to 400 m, which is further than both bee families. Main conclusions: A diverse array of wild and managed flower visitors can transport viable pollen from a pollen source to at least 400 m. Knowledge of the differences in transport distances among generalist pollinators in human-modified environments is crucial to understand the potential extent to which (1) pollen transport can facilitate gene flow and (2) unwanted hybridization may occur between crops and related weeds.