Effects of multiple stressors on the health of different bee species

Abstract

In recent decades, concerns about declining bee populations have multiplied, including managed honey bees and wild bees. The reasons for this decline have been widely discussed and researched during the last decades. In addition to parasites and pathogens, the use of agrochemicals and diminishing food resource quality and quantity are suspected to be the principal factors behind dwindling bee populations. In the past, most studies focussed on the effects of single stressors; however, the focus on studying the impact of combined stressors has recently increased, as stressors may operate interactively. For example, the quality and quantity of bee nutrition may affect the susceptibility of bees to pathogens or agrochemicals, and mixtures of some pesticides may act synergistically rather than additively.
In this dissertation, three studies were conducted to investigate the combined effects of insecticides, fungicides and nutrition on three commercially used bee species (Apis mellifera L., Bombus terrestris L., Osmia bicornis L.) via laboratory and semi-field experiments. The three bee species researched in this dissertation, namely the highly eusocial honey bee A. mellifera, the primitively eusocial buff-tailed bumble bee B. terrestris and the solitary mason bee O. bicornis, have different levels of sociality and are therefore well suited as model organisms for this scientific issue.
The first part of this thesis (Chapter II) compares the responses of the three bee species (A. mellifera, B. terrestris, O. bicornis) to exposure to the fungicide prochloraz, the insecticide chlorantraniliprole and their mixture with different nutritional resources (sugar only, sugar with amino acids or pollen) under laboratory conditions. Survival, sensitivity, enzyme activity and abdomen protein content were analysed. All bee species were affected by their diet as well as the plant protection product used, but they responded differently. A. mellifera benefitted the most from additional amino acids in their diet, alone and in combination with plant protection products, whereas O. bicornis benefitted more from a pollen diet than from an amino acid diet, and B. terrestris benefitted from both pollen and amino acids. The results indicate that the sensitivity of bee species to agrochemicals is affected by diet and that the sugar-only diet in particular can increase bee species’ sensitivity to pesticides.
As laboratory studies only provide limited information regarding real bee populations in the field, we conducted semi-field studies in the third and fourth parts of this thesis (Chapter III and Chapter IV). Chapter III reports the results of a semi-field experiment with Bombus terrestris colonies exposed to the same pesticides as in the laboratory experiment (tank mixture containing the insecticide chlorantraniliprole and the fungicide prochloraz) either in monoculture-managed lupin (Lupinus albus L.) as high-pollen protein recourse (monofloral) or in the presence of an additional flower mixture (polyfloral). Colony growth, worker mortality, new queen and drone production and the fungal microbiome of B. terrestris were monitored. The tank mixture had a significant effect on worker mortality in polyfloral variants. However, this exerted no effect on the number of brood cells (i.e., egg, larvae and pupae cells), as there were significantly more brood cells in polyfloral treatments. No differences were discovered in the number or weight of new queens or drones. This likely indicates that neither the pesticide application nor the monofloral flowering resources have a long-term effect on B. terrestris populations.
In a second semi-field study (Chapter IV), honey bee colonies (A. mellifera) were exposed to a mixture of the fungicide prochloraz and the neonicotinoid insecticide thiacloprid in monofloral maize (Zea mays L.), in monofloral Phacelia tanacetifolia Benth. or in maize with an additional flowering mixture (flowering strip). Colony development, the longevity of newly hatched worker bees, body and head weight and the enzyme activity of acetylcholinesterase and P450 reductase were also investigated. The capping rate of colonies in treated maize was significantly reduced compared to treated flowering strips and treated Phacelia. The effect of pesticide exposure on the longevity of adults differed significantly between maize and Phacelia, with flowering strips being intermediate. Pesticide exposure slightly increased the body weight of worker honey bees in all nutritional statuses, except for Phacelia. The enzyme activity of acetylcholinesterase and P450 reductase exhibited significantly different responses to pesticide exposure between maize and Phacelia, but not between maize and flowering strips.
The results of the three studies in this thesis highlight the importance of sufficient nutrition to mitigate the negative effects of pesticides. However, the specific results differ based on distinct bee species and laboratory or field conditions. This dissertation emphasises the importance of essential amino acids and protein content for A. mellifera. However, other nutrients appear to be important as well, especially for O. bicornis and B. terrestris. We recommend maintaining and promoting diverse flowering strips in agricultural landscapes and even near high-pollen protein crops so that bees can choose the suitable nutrients in pollen and nectar.

This dissertation was only published as a printed edition.