SciCombinator

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Concept: Pollination syndrome

203

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

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

172

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

161

With more than 80% of flowering plant species specialized for animal pollination, understanding how wild pollinators utilize resources across environments can encourage efficient planting and maintenance strategies to maximize pollination and establish resilience in the face of environmental change. A fundamental question is how generalist pollinators recognize “flower objects” in vastly different ecologies and environments. On one hand, pollinators could employ a specific set of floral cues regardless of environment. Alternatively, wild pollinators could recognize an exclusive signature of cues unique to each environment or flower species. Hoverflies, which are found across the globe, are one of the most ecologically important alternative pollinators after bees and bumblebees. Here, we have exploited their cosmopolitan status to understand how wild pollinator preferences change across different continents. Without employing any a priori assumptions concerning the floral cues, we measured, predicted, and finally artificially recreated multimodal cues from individual flowers visited by hoverflies in three different environments (hemiboreal, alpine, and tropical) using a field-based methodology. We found that although “flower signatures” were unique for each environment, some multimodal lures were ubiquitously attractive, despite not carrying any reward, or resembling real flowers. While it was unexpected that cue combinations found in real flowers were not necessary, the robustness of our lures across insect species and ecologies could reflect a general strategy of resource identification for generalist pollinators. Our results provide insights into how cosmopolitan pollinators such as hoverflies identify flowers and offer specific ecologically based cues and strategies for attracting pollinators across diverse environments.

Concepts: Natural environment, Pollination, Flower, Pollinator decline, Pollination syndrome, Pollen, Bee, Self-pollination

139

The causes of declines in bees and other pollinators remains an on-going debate. While recent attention has focussed upon pesticides, other environmental pollutants have largely been ignored. Aluminium is the most significant environmental contaminant of recent times and we speculated that it could be a factor in pollinator decline. Herein we have measured the content of aluminium in bumblebee pupae taken from naturally foraging colonies in the UK. Individual pupae were acid-digested in a microwave oven and their aluminium content determined using transversely heated graphite furnace atomic absorption spectrometry. Pupae were heavily contaminated with aluminium giving values between 13.4 and 193.4 μg/g dry wt. and a mean (SD) value of 51.0 (33.0) μg/g dry wt. for the 72 pupae tested. Mean aluminium content was shown to be a significant negative predictor of average pupal weight in colonies. While no other statistically significant relationships were found relating aluminium to bee or colony health, the actual content of aluminium in pupae are extremely high and demonstrate significant exposure to aluminium. Bees rely heavily on cognitive function and aluminium is a known neurotoxin with links, for example, to Alzheimer’s disease in humans. The significant contamination of bumblebee pupae by aluminium raises the intriguing spectre of cognitive dysfunction playing a role in their population decline.

Concepts: Statistics, Pollination, Pollinator decline, Pollination syndrome, Bee, Bumblebee, Pollinator, Soil contamination

72

Bumblebees secrete a substance from their tarsi wherever they land, which can be detected by conspecifics. These secretions are referred to as scent-marks, which bumblebees are able to use as social cues. Although it has been found that bumblebees can detect and associate scent-marks with rewarding or unrewarding flowers, their ability at discriminating between scent-marks from bumblebees of differing relatedness is unknown. We performed three separate experiments with bumblebees (Bombus terrestris), where they were repeatedly exposed to rewarding and unrewarding artificial flowers simultaneously. Each flower type carried scent-marks from conspecifics of differing relatedness or were unmarked. We found that bumblebees are able to distinguish between 1. Unmarked flowers and flowers that they themselves had scent-marked, 2. Flowers scent-marked by themselves and flowers scent-marked by others in their nest (nestmates), and 3. Flowers scent-marked by their nestmates and flowers scent-marked by non-nestmates. The bumblebees found it more difficult to discriminate between each of the flower types when both flower types were scent-marked. Our findings show that bumblebees have the ability to discriminate between scent-marks of conspecifics, which are potentially very similar in their chemical composition, and they can use this ability to improve their foraging success.

Concepts: Pollination, Flower, Pollinator decline, Pollination syndrome, Bee, Bumblebee, Bombus terrestris, Bumblebees

52

Multiple interacting factors drive recent declines in wild and managed bees, threatening their pollination services. Widespread and intensive monitoring could lead to more effective management of wild and managed bees. However, tracking their dynamic populations is costly. We tested the effectiveness of an inexpensive, noninvasive and passive acoustic survey technique for monitoring bumble bee behavior and pollination services. First, we assessed the relationship between the first harmonic of the flight buzz (characteristic frequency) and pollinator functional traits that influence pollination success using flight cage experiments and a literature search. We analyzed passive acoustic survey data from three locations on Pennsylvania Mountain, Colorado to estimate bumble bee activity. We developed an algorithm based on Computational Auditory Scene Analysis that identified and quantified the number of buzzes recorded in each location. We then compared visual and acoustic estimates of bumble bee activity. Using pollinator exclusion experiments, we tested the power of buzz density to predict pollination services at the landscape scale for two bumble bee pollinated alpine forbs (Trifolium dasyphyllum and T. parryi). We found that the characteristic frequency was correlated with traits known to affect pollination efficacy, explaining 30-52% of variation in body size and tongue length. Buzz density was highly correlated with visual estimates of bumble bee density (r = 0.97), indicating that acoustic signals are predictive of bumble bee activity. Buzz density predicted seed set in two alpine forbs when bumble bees were permitted access to the flowers, but not when they were excluded from visiting. Our results indicate that acoustic signatures of flight can be deciphered to monitor bee activity and pollination services to bumble bee pollinated plants. We propose that applications of this technique could assist scientists and farmers in rapidly detecting and responding to bee population declines.

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

52

Insects use several senses to forage, detecting floral cues such as color, shape, pattern, and volatiles. We report a formerly unappreciated sensory modality in bumblebees (Bombus terrestris), detection of floral electric fields. These fields act as floral cues, which are affected by the visit of naturally charged bees. Like visual cues, floral electric fields exhibit variations in pattern and structure, which can be discriminated by bumblebees. We also show that such electric field information contributes to the complex array of floral cues that together improve a pollinator’s memory of floral rewards. Because floral electric fields can change within seconds, this sensory modality may facilitate rapid and dynamic communication between flowers and their pollinators.

Concepts: Sensory system, Pollination, Pollinator decline, Pollination syndrome, Bee, Bumblebee, Pollinator, Pollinators