Dead Bees under Lime Trees

We have a lime tree in our garden, and another in the lane leading to the school, and for many days past we have found on the path under the lime tree quantities of dead bumble-bees. I have enclosed some of them for your inspection. It will be seen that there is only the shell left of each bee's thorax. A curious thing is that, although the inside is completely scooped out, their legs move long after they fall on the ground. Can you tell us what it is that kills them?  Wm. Oliver, Westbury School, Shrewsbury.

British Bee Journal 1907

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Dead bees under lime trees 

When the limes were in flower in England last year, many people were disturbed to see bees lying dead, paralysed or " drunk " under the trees. There were reports that the ground was covered with dead honeybees—or, more often, with dead bumblebees—and some other species were also affected. The damage was variously attributed to the nectar or pollen of the lime trees, to toxic chemicals, or to more mysterious sources. Most reports came from localities where the soil is quickly drained, and in any case the 1976 summer was exceptionally dry. The cause of this damage seems to be rather little known, although it was established in 1960. 

The toxicity of the nectar and pollen of lime (Tilia) species is due to certain sugars in them, which are present in abnormally high amounts in dry years. These sugars disturb carbohydrate metabolism in bees of various species. The chief culprit is mannose, which von Frisch found was strongly toxic to honeybees, in 1931. Mannose is a common sugar, utilizable by many organisms (including man), but not by certain insects, in which it produces a " metabolic disease ". The first stage in mannose metabolism is its transformation into mannose-6-phosphate by the enzyme hexokinase,which is present in bees. The second stage is the conversion of the mannose-6-phosphate (which is itself toxic to them) into fructose-6-phosphate by the enzyme mannosephosphate isomerase. But honeybees and some other bees have no more than a trace of this enzyme; in these bees, therefore, mannose-6-phosphate is formed but is not broken down again; it accumulates in the digestive system. More than this,hexokinase produces a faster reaction with mannose than with glucose and fructose,so the latter non-toxic sugars are not metabolized in the presence of mannose, and the sugar level in the blood falls. Honeybees fed experimentally on the sugars galactose and rhamnose, as well as mannose, died similarly; the toxic sugars increased in the blood and thorax, while the levels of glucose and fructose dropped. The thoracic muscles were unable to function, so the bees could not move their wings and legs—and appeared paralysed. This is what had happened to the dead and " drunk " bees under lime trees. Some wild bees are more affected than honeybees, possibly because of their different feeding habits with regard to nectar and pollen. The lime species most implicated seem to be Tilia tomentosa (argentea) and itscultivar T. petiolaris, T. orbicularis and T. cordata. T. miqiieliana has been recom-mended as a late species for planting instead of T. petiolaris, for this reason. The severity of the effect varies from season to season, and from place to place,being greatest in dry years and on well drained soils. The following facts have been reported from Switzerland. In the Innertkirchen region of Canton Bern, colonies of honey bees were weakened considerably during the 1922 lime flowering; according to some reports this happened every year. In 1925 a beekeeper in Herbligen said he lost 50% of his flying bees during the flowering of Tilia argentea. In 1943 many paralysed bees were found in an apiary at Liebefeld-Bern, at the end of June and throughout July. They were crawling on the gravel paths, dragging the abdomen and unable to fly. 

Eva Crane 1977

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