SciCombinator

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Concept: Pollinator decline

550

Recent declines in honey bee populations and increasing demand for insect-pollinated crops raise concerns about pollinator shortages. Pesticide exposure and pathogens may interact to have strong negative effects on managed honey bee colonies. Such findings are of great concern given the large numbers and high levels of pesticides found in honey bee colonies. Thus it is crucial to determine how field-relevant combinations and loads of pesticides affect bee health. We collected pollen from bee hives in seven major crops to determine 1) what types of pesticides bees are exposed to when rented for pollination of various crops and 2) how field-relevant pesticide blends affect bees' susceptibility to the gut parasite Nosema ceranae. Our samples represent pollen collected by foragers for use by the colony, and do not necessarily indicate foragers' roles as pollinators. In blueberry, cranberry, cucumber, pumpkin and watermelon bees collected pollen almost exclusively from weeds and wildflowers during our sampling. Thus more attention must be paid to how honey bees are exposed to pesticides outside of the field in which they are placed. We detected 35 different pesticides in the sampled pollen, and found high fungicide loads. The insecticides esfenvalerate and phosmet were at a concentration higher than their median lethal dose in at least one pollen sample. While fungicides are typically seen as fairly safe for honey bees, we found an increased probability of Nosema infection in bees that consumed pollen with a higher fungicide load. Our results highlight a need for research on sub-lethal effects of fungicides and other chemicals that bees placed in an agricultural setting are exposed to.

Concepts: Insect, Beekeeping, Pesticide, Pollination, Flower, Pollinator decline, Bumblebee, Pollinator

218

This study measured part of the in-hive pesticide exposome by analyzing residues from live in-hive bees, stored pollen, and wax in migratory colonies over time and compared exposure to colony health. We summarized the pesticide burden using three different additive methods: (1) the hazard quotient (HQ), an estimate of pesticide exposure risk, (2) the total number of pesticide residues, and (3) the number of relevant residues. Despite being simplistic, these models attempt to summarize potential risk from multiple contaminations in real-world contexts. Colonies performing pollination services were subject to increased pesticide exposure compared to honey-production and holding yards. We found clear links between an increase in the total number of products in wax and colony mortality. In particular, we found that fungicides with particular modes of action increased disproportionally in wax within colonies that died. The occurrence of queen events, a significant risk factor for colony health and productivity, was positively associated with all three proxies of pesticide exposure. While our exposome summation models do not fully capture the complexities of pesticide exposure, they nonetheless help elucidate their risks to colony health. Implementing and improving such models can help identify potential pesticide risks, permitting preventative actions to improve pollinator health.

Concepts: Insect, Risk, Risk management, Honey bee, Beekeeping, Pesticide, Pollination, Pollinator decline

216

Wild bees are highly valuable pollinators. Along with managed honey bees, they provide a critical ecosystem service by ensuring stable pollination to agriculture and wild plant communities. Increasing concern about the welfare of both wild and managed pollinators, however, has prompted recent calls for national evaluation and action. Here, for the first time to our knowledge, we assess the status and trends of wild bees and their potential impacts on pollination services across the coterminous United States. We use a spatial habitat model, national land-cover data, and carefully quantified expert knowledge to estimate wild bee abundance and associated uncertainty. Between 2008 and 2013, modeled bee abundance declined across 23% of US land area. This decline was generally associated with conversion of natural habitats to row crops. We identify 139 counties where low bee abundances correspond to large areas of pollinator-dependent crops. These areas of mismatch between supply (wild bee abundance) and demand (cultivated area) for pollination comprise 39% of the pollinator-dependent crop area in the United States. Further, we find that the crops most highly dependent on pollinators tend to experience more severe mismatches between declining supply and increasing demand. These trends, should they continue, may increase costs for US farmers and may even destabilize crop production over time. National assessments such as this can help focus both scientific and political efforts to understand and sustain wild bees. As new information becomes available, repeated assessments can update findings, revise priorities, and track progress toward sustainable management of our nation’s pollinators.

Concepts: Agriculture, Insect, United States, Beekeeping, Pollinator decline, Bee, Bumblebee, Pollinator

214

The causes of bee declines remain hotly debated, particularly the contribution of neonicotinoid insecticides. In 2013 the UK’s Food & Environment Research Agency made public a study of the impacts of exposure of bumblebee colonies to neonicotinoids. The study concluded that there was no clear relationship between colony performance and pesticide exposure, and the study was subsequently cited by the UK government in a policy paper in support of their vote against a proposed moratorium on some uses of neonicotinoids. Here I present a simple re-analysis of this data set. It demonstrates that these data in fact do show a negative relationship between both colony growth and queen production and the levels of neonicotinoids in the food stores collected by the bees. Indeed, this is the first study describing substantial negative impacts of neonicotinoids on colony performance of any bee species with free-flying bees in a field realistic situation where pesticide exposure is provided only as part of normal farming practices. It strongly suggests that wild bumblebee colonies in farmland can be expected to be adversely affected by exposure to neonicotinoids.

Concepts: Insect, Honey bee, Pollinator decline, Bee, Bumblebee, Insecticide, Neonicotinoid, Imidacloprid

194

Central place foragers, such as pollinating bees, typically develop circuits (traplines) to visit multiple foraging sites in a manner that minimizes overall travel distance. Despite being taxonomically widespread, these routing behaviours remain poorly understood due to the difficulty of tracking the foraging history of animals in the wild. Here we examine how bumblebees (Bombus terrestris) develop and optimise traplines over large spatial scales by setting up an array of five artificial flowers arranged in a regular pentagon (50 m side length) and fitted with motion-sensitive video cameras to determine the sequence of visitation. Stable traplines that linked together all the flowers in an optimal sequence were typically established after a bee made 26 foraging bouts, during which time only about 20 of the 120 possible routes were tried. Radar tracking of selected flights revealed a dramatic decrease by 80% (ca. 1500 m) of the total travel distance between the first and the last foraging bout. When a flower was removed and replaced by a more distant one, bees engaged in localised search flights, a strategy that can facilitate the discovery of a new flower and its integration into a novel optimal trapline. Based on these observations, we developed and tested an iterative improvement heuristic to capture how bees could learn and refine their routes each time a shorter route is found. Our findings suggest that complex dynamic routing problems can be solved by small-brained animals using simple learning heuristics, without the need for a cognitive map.

Concepts: Honey bee, Pollination, Flower, Pollinator decline, Pollination syndrome, Bee, Bumblebee, Pollinator

191

Agricultural land use results in direct biodiversity decline through loss of natural habitat, but may also cause indirect cross-habitat effects on conservation areas. We conducted three landscape-scale field studies on 67 sites to test the hypothesis that mass flowering of oilseed rape (Brassica napus) results in a transient dilution of bees in crop fields, and in increased competition between crop plants and grassland plants for pollinators. Abundances of bumble-bees, which are the main pollinators of the grassland plant Primula veris, but also pollinate oilseed rape (OSR), decreased with increasing amount of OSR. This landscape-scale dilution affected bumble-bee abundances strongly in OSR fields and marginally in grasslands, where bumble-bee abundances were generally low at the time of Primula flowering. Seed set of Primula veris, which flowers during OSR bloom, was reduced by 20 per cent when the amount of OSR within 1 km radius increased from 0 to 15 per cent. Hence, the current expansion of bee-attractive biofuel crops results in transient dilution of crop pollinators, which means an increased competition for pollinators between crops and wild plants. In conclusion, mass-flowering crops potentially threaten fitness of concurrently flowering wild plants in conservation areas, despite the fact that, in the long run, mass-flowering crops can enhance abundances of generalist pollinators and their pollination service.

Concepts: Agriculture, Pollination, Brassica, Flower, Pollinator decline, Pollination syndrome, Bumblebee, Pollinator

173

The daylily (Hemerocallis fulva) and nightlily (H. citrina) are typical examples of a butterfly-pollination system and a hawkmoth-pollination system, respectively. H. fulva has diurnal, reddish or orange-colored flowers and is mainly pollinated by diurnal swallowtail butterflies. H. citrina has nocturnal, yellowish flowers with a sweet fragrance and is pollinated by nocturnal hawkmoths. We evaluated the relative roles of flower color and scent on the evolutionary shift from a diurnally flowering ancestor to H. citrina. We conducted a series of experiments that mimic situations in which mutants differing in either flower color, floral scent or both appeared in a diurnally flowering population. An experimental array of 6 × 6 potted plants, mixed with 24 plants of H. fulva and 12 plants of either F1 or F2 hybrids, were placed in the field, and visitations of swallowtail butterflies and nocturnal hawkmoths were recorded with camcorders. Swallowtail butterflies preferentially visited reddish or orange-colored flowers and hawkmoths preferentially visited yellowish flowers. Neither swallowtail butterflies nor nocturnal hawkmoths showed significant preferences for overall scent emission. Our results suggest that mutations in flower color would be more relevant to the adaptive shift from a diurnally flowering ancestor to H. citrina than that in floral scent.

Concepts: Fruit, Pollination, Flower, Pollinator decline, Pollination syndrome, Pollen, Flowers, Stamen

171

Floral displays are under selection to both attract pollinators and deter antagonists. Here we show that a common floral trait, a nectar guide pattern, alters the behavior of bees that can act opportunistically as both pollinators and as antagonists. Generally, bees access nectar via the floral limb, transporting pollen through contact with the plant’s reproductive structures; however bees sometimes extract nectar from a hole in the side of the flower that they or other floral visitors create. This behavior is called “nectar robbing” because bees may acquire the nectar without transporting pollen. We asked whether the presence of a symmetric floral nectar guide pattern on artificial flowers affected bumble bees' (Bombus impatiens) propensity to rob or access nectar “legitimately.” We discovered that nectar guides made legitimate visits more efficient for bees than robbing, and increased the relative frequency of legitimate visits, compared to flowers lacking nectar guides. This study is the first to show that beyond speeding nectar discovery, a nectar guide pattern can influence bees' flower handling in a way that could benefit the plant.

Concepts: Pollination, Plant morphology, Flower, Pollinator decline, Pollination syndrome, Pollen, Bee, Bumblebee

170

In the past decade, accumulating evidence of pollinator decline has raised concerns regarding the functioning of terrestrial ecosystems and the sustainability of crop production. Although land-use changes have been advanced as the major causes, the affinities of most wild pollinators with the main land-use types remain unknown. Filling this gap in our knowledge is a prerequisite to improving conservation and management programmes.

Concepts: Biodiversity, Pollination, Pollinator decline, Pollination syndrome, Bee, Pollinator, Land use

94

Insect pollinators such as bumblebees play a vital role in many ecosystems, so it is important to understand their foraging movements on a landscape scale. We used harmonic radar to record the natural foraging behaviour of Bombus terrestris audax workers over their entire foraging career. Every flight ever made outside the nest by four foragers was recorded. Our data reveal where the bees flew and how their behaviour changed with experience, at an unprecedented level of detail. We identified how each bee’s flights fit into two categories-which we named exploration and exploitation flights-examining the differences between the two types of flight and how their occurrence changed over the course of the bees' foraging careers. Exploitation of learned resources takes place during efficient, straight trips, usually to a single foraging location, and is seldom combined with exploration of other areas. Exploration of the landscape typically occurs in the first few flights made by each bee, but our data show that further exploration flights can be made throughout the bee’s foraging career. Bees showed striking levels of variation in how they explored their environment, their fidelity to particular patches, ratio of exploration to exploitation, duration and frequency of their foraging bouts. One bee developed a straight route to a forage patch within four flights and followed this route exclusively for six days before abandoning it entirely for a closer location; this second location had not been visited since her first exploratory flight nine days prior. Another bee made only rare exploitation flights and continued to explore widely throughout its life; two other bees showed more frequent switches between exploration and exploitation. Our data shed light on the way bumblebees balance exploration of the environment with exploitation of resources and reveal extreme levels of variation between individuals.

Concepts: Honey bee, Pollinator decline, Bee, Bumblebee, Pollinator, Apidae, Pollinators, Foraging