Short Communication |
Corresponding author: Sydney A. Cameron ( scameron@life.illinois.edu ) Academic editor: Jack Neff
© 2019 Sydney A. Cameron, Sarah A. Corbet, James B. Whitfield.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Cameron SA, Corbet SA, Whitfield JB (2019) Bumble bees (Hymenoptera: Apidae: Bombus terrestris) collecting honeydew from the giant willow aphid (Hemiptera: Aphididae). Journal of Hymenoptera Research 68: 75-83. https://doi.org/10.3897/jhr.68.30495
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Only rarely have bumble bees (Bombus) been observed collecting honeydew from aphids (Aphididae) feeding on phloem sap. This behavior may be rare because the percentage of sugar in honeydew egested from aphids is generally well below the sugar concentration in floral nectars preferred by bumble bees. Nonetheless, in August 2018, near St. Buryan, Penzance, Cornwall, UK (56.0602N; -5.6034W) we observed large numbers of wild Bombus terrestris (Linnaeus) collecting honeydew from a colony of the giant willow aphid Tuberolachnus salignus Gmelin feeding on the stems of the willow Salix alba. Unlike aphid-tending ants, who glean fresh honeydew directly from the aphid anal opening, the bumble bees were collecting honeydew from leaf litter below the aphid colony. We hypothesized that honeydew collected from exposed ground surfaces was more concentrated due to evaporation under ambient conditions than that released directly from the anus (fresh honeydew). We thus monitored sugar concentrations of fresh honeydew and compared them with the concentrations of the crop contents of worker bumble bees foraging from the leaf litter. Our data show that the concentration of sugar in fresh honeydew was as much as 10% w/w lower than that collected from leaf surfaces, as measured from the crop contents of foragers. The unusually hot, dry weather in Cornwall may have enhanced evaporative concentration of honeydew while restricting floral nectar sources, thus favoring honeydew collection by B. terrestris, a generalist bumble bee forager.
Tuberolachnus salignus , Salix alba , solute concentrations, foraging behavior
Most bee species depend on carbohydrates, primarily sucrose, glucose and fructose (
Nonetheless, in Aug 2018 we observed large numbers of Bombus terrestris gleaning honeydew from surfaces below an aphid colony feeding on willow (Salix) in Southwest Cornwall, UK. The rarity of this behavior in bumble bees suggested that abnormal environmental conditions might be involved as a result of an unusually dry summer. Drought and relatively high temperature conditions are known to reduce total sugar content in nectar – three times less in some flower species – leading to decreased flower visitation rates by bumble bees (
Honeydew can be collected either directly from the anus of aphids (common in ants) or after falling onto surfaces below an aphid colony (
In early August 2018, during an extended period of unusually hot, dry weather, we heard loud buzzing in the vicinity of a willow shrub growing in a cultivated flower garden at Boskenna Farm, St. Buryan, Penzance, Cornwall, UK (56.0602N; -5.6034W). On Aug 6, from dawn to dusk (0500-2130 BST), we observed B. terrestris (Linnaeus) females and males collecting honeydew that rained down approximately 1.2 m onto leaf litter directly beneath a colony of the cosmopolitan (
At 4-hr intervals during the day (5:45 am, 9:45 am, 1:55 pm, 5:45 pm and 9:15 pm British Summer Time) we made spot counts of all bumble bees on the ground within a ~1.2 m2 area underneath the aphid colony (Fig.
A Giant willow aphids (Tuberolachnus salignus) on a branch of Salix alba; larger aphids range from 5.1–5.7 mm B Bombus terrestris collecting honeydew from leaf litter beneath several branches bearing the aphids C holding a plastic plate beneath the aphid colonies to collect honeydew droplets D collecting honeydew droplets from the plate using a 5 μl glass capillary tube E compressing a worker bumble bee to force regurgitation of crop contents onto the plate F using a refractometer to measure solute concentration of honeydew.
During each of the five time intervals (when bees were foraging), we collected a random sample of 5-6 live bees foraging on the honeydew using 15-cm long forceps. They were kept cool on ice and taken indoors for measurement of solute concentration in the crop. To measure crop solute concentration, we placed each worker bee onto a clean unwettable 12 x 15 cm plastic plate, holding the bee in place with a foam plunger (Fig.
Aphids were identified using
The total number of B. terrestris (workers and males) gleaning honeydew from the surfaces of leaf litter changed through the day, with the largest number of bees arriving early, and numbers declining through the day (Fig.
Solute concentrations in honeydew egested freshly by the aphids were consistently low, ranging from 12% in early morning to 18% in the afternoon and 16% by sunset (Fig.
Why were so many B. terrestris workers collecting aphid honeydew on this occasion? Our finding that bumble bee crop contents were more concentrated than fresh honeydew indicates that bumble bees were not solely collecting the very dilute fresh honeydew. The abnormal environmental conditions at the time likely played a part in this rarely observed behavior. The summer of 2018 was the hottest in England since records began, and Cornwall was under significant drought stress, with no significant rainfall from June to August. It is therefore likely that food and water resources from flowers were much reduced, affecting pollinator attractiveness. Bumble bees could enhance their food reward by collecting the more concentrated honeydew. The high temperatures and low relative humidity would cause rapid evaporative concentration of fallen honeydew droplets, perhaps raising the solute concentration to a level acceptable to bumble bees. Their crops may also have contained sugar solutions from other sources. It is notable that
While we did not quantify the amount of honeydew falling onto the leaf litter, it was audible as it rained down onto the dry leaves in the early morning when fewer bees were buzzing. The honeydew droplets were between 3 and 5 µl, as estimated when drawing droplets into 5 µl capillary tubes. Multiple droplets per second fell from the aphids onto the plastic tray held beneath the colony. As the aphids continued to feed and release honeydew from dawn to dusk, they provided a reward bonanza for the bumble bees at this time.
Global climate change leading to drought and temperature stress has led to multiple reports that wildflowers important to bees experience reduced nectar production with lower sugar quantity (
Bombus terrestris, a short tongued bumble bee, was the sole bumble bee species seen collecting honeydew at our site, even though several other species are common in the area, including the long-tongued B. pascuorum (Scopoli). This might be explained by the fact that B. terrestris (subgenus Bombus) is a generalist bumble bee, similar to other members of the subgenus Bombus sensu stricto, and preadapted to foraging on a wide array of food sources. In fact, two of only three published observations of bumble bees collecting aphid honeydew in North America (
No other bees, such as honey bees or solitary bees, collected honeydew at the site, nor did we see any ants, although it has been reported that T. salignus colonies in the UK are often tended by ants (
We are indebted to Thelma and Anthony Woodward for alerting us to the bumble bees and wasps buzzing around the Salix alba in their garden. Their hospitality was invaluable to the study. We thank Joan Meiners and Jack Neff for their knowledgeable input and helpful comments on the manuscript.