The macronutrient regulation of adult worker honeybees

Lead Research Organisation: Royal Botanic Gardens Kew
Department Name: Natural Capital and Plant Health

Abstract

World agriculture relies on insects to pollinate flowering crops, especially soft fruit, vegetable, and nut crops, that are increasingly forming the basis of most human diets. As our diet shifts from grains and cereals to including more vegetables and fruits, the demand for these services continues to grow in step with the world's population. In fact, human consumption of fruits, nuts and vegetables that require pollination has increased as much as 300% in the past 50 years. In addition, other crops that improve seed set when pollinated such as oilseed rape are important for food but are also potential biofuels. Pollinators, and their well-being, are important to our future health and survival.

Domesticated bees are the most important pollinators used in world agriculture. Commercial honeybee keepers maintain thousands of colonies, transporting them to orchards or other agricultural field settings to perform pollination services. Commercial beekeepers often struggle to find enough pollen to feed their colonies, especially at times of year when natural forage is scarce. Insufficient nutrition is one of the main factors for the poor health in honeybee colonies that are beset by pathogens and parasites, as well as exposed to a diversity of agricultural pesticides. In the past 20 years, beekeepers have started to rely on feeding colonies with commercial pollen substitutes but these substitutes are not scientifically formulated and do not have all of the essential nutrients bees need.

Our recent BBSRC-funded research investigated the adult worker honeybee's nutritional needs. We found that adult worker bees self-select proportions of protein and carbohydrate and that their demands for protein and carbohydrate change as a function of their caste. In addition, foods high in protein or essential amino acids reduce survival. We also found that the proportion of essential amino acids in diet affected the regulation of protein intake. Our recent work indicates that diets too high in fat shorten adult worker bee lifespan, and that the proportions of essential fatty acids in food affect learning performance and glandular development in adult worker honeybees.

Here, we propose to extend our research on bee nutrition to identify how bees regulate their protein, fat, and sterols. Our experiments will also examine how sources of proteins, fats, and sterols can be combined to produce mixtures that meet the honeybee's needs for essential nutrients. We will start by testing the digestibility of several potential protein sources and their effect on the intake of food in adult worker bees. Extending our previous research, we will test how the proportion of essential amino acids in dietary protein affects the total amount of protein bees consume. Fat is an important nutrient for bees, and makes up nearly 30% of the dry weight of royal jelly (i.e. glandular secretions fed to larvae and the queen) but is only found at between 5-7% of the dry weight of pollen. In our proposed experiments, we will identify the relative ratio of protein to fat needed by adult worker bees in the presence and absence of brood. Bees also need a dietary source of phytosterols that are found in pollen. We will also perform experiments that test how much of these sterols adult worker bees need to rear brood successfully. Our experiments will lead to a final test of a combination of protein, fat, carbohydrate, and sterols in whole colonies compared to the performance of bees fed with natural pollen. With this information, we will be able to provide advice to beekeepers on the materials and their combinations that can be used to formulate substitutes for pollen when pollen is unavailable.

Technical Summary

Pollination provided by domesticated honeybees is critical in agricultural systems where flowering plants are obligated to outcross (e.g. apples). Providing sufficient pollen forage for bees is a challenge in landscapes under heavy agricultural cultivation. Beekeepers face many difficulties such as disease, parasites, and pesticides that are exacerbated by poor nutrition. In response, beekeepers often feed colonies with substitutes for pollen that are indigestible or do not provide all of the essential nutrients bees need. Here, we propose to extend our work on bee nutrition to advise beekeepers about ways they can supplement bee diets when pollen is scarce. Our proposal has three main aims: (1) to identify how bees digest and regulate their intake of protein relative to other nutrients; (2) to identify the optimal amount of essential fats and sterols bees need in diet; and (3) test a predicted 'optimal' mixture of macronutrients on entire colonies. We will start out by testing the digestibility of potential protein sources. Using the Geometric Framework for nutrition, we will measure how the proportions of essential amino acids in food affect the regulation of protein intake. We will also identify the optimal protein-to-fat ratio for honeybees. These experiments will include manipulations of the relative proportions of the total amount of the two essential fatty acids (linoleic and a-linolenic acid) in diet that we know are important for bee development and performance. Critically, we will identify the amount of 24-methylene cholesterol (an essential sterol) needed by adult worker honeybees with and without brood. Finally, we will test our predicted optimal combination of these materials in whole colonies against the performance of colonies fed with natural, honeybee collected pollen. This information will enable beekeepers to feed bees with the best substrates and their correct proportions in the absence of pollen and hence will impact world agriculture.

Planned Impact

World agriculture relies on pollinators for the production of soft fruits, nuts, seeds, and vegetables. In large scale agriculture such as almond orchards in California, pollination services are primarily accomplished by honeybee colonies that are transported to orchards and fields by the millions during flowering. Commercial beekeepers are paid for each colony they bring to a field site. Prior to flowering, these colonies may not have access to much pollen, which means it is difficult to build up the colony's size and strengthen health. To overcome pollen dearth, beekeepers in the past 30 years have started to use bee feeds made from grains like soya beans: products that are inexpensive and easy to obtain. The base products are purchased from beekeeping suppliers, mixed with sugar solutions (e.g. high fructose corn syrup) in the field, and then provided to the bees as a patty or a liquid food within the colony. Beekeepers sometimes make and mix their own formulations. A major problem with these feeds is the fact that they do not provide essential nutrients (e.g. correct fatty acids and sterols). These base materials (e.g. soy) are also difficult for bees to digest and have been reported to cause dysentery. They are also not formulated in a way that optimizes combinations of macronutrients for honeybees. In fact, to make these substances palatable to bees, beekeepers add ~5-20% honeybee collected pollen to the mix, but this is very expensive and has the potential to spread disease and expose bees to pesticides.

Our proposed research will have a large impact on the beekeeping industry and agriculture. At present, there is a pressing need in the commercial beekeeping industry for bee foods that are substitutes for pollen. To obtain natural forage for their bees, beekeepers also transport their colonies to places where forage is available. This is expensive and stressful for bees. Having a substitute for pollen that did not require the addition of bee collected pollen would reduce the need to transport bees to forage and reduce risk associated with exposure to pathogens from bee collected pollen. Native bees compete with honeybees for access to natural pollen and nectar; a pollen substitute for honeybees would also reduce competition for floral resources in natural habitats and improve wild bee populations.
Presenting our research at international beekeeping conferences and local meetings, we have realized that beekeepers worldwide are very keen to find a way to improve the nutrition of their colonies. This need motivated us to focus our nutrition work towards the goal of producing food that could be used when pollen was unavailable. The research described in our proposal will provide the following: 1) specific information about the nutritional needs of honeybees; 2) information about raw materials that can be used as food in bee colonies; 3) insight into nutrient balancing by social insects, especially for proteins, fats, and sterols. As part of our impact plan, we will begin the process of commercialization of the information we obtain here by applying for BBSRC Follow on Funding and starting a spin-out company that will develop and orchestrate the production of bee feeds. The research described in this proposal will guide our potential future commercialization of this information. The data we produce from this work will also be published in scientific journals and interpreted and made available to beekeepers via a website managed in association with the British Beekeeping Association. This information will permit beekeepers to improve upon their methods of feeding and will improve pollination services for agricultural crops worldwide.
 
Description Sterol chemistry of floral resources differs across plant species and is phylogenetically linked across substitution at the 24 position - 24 methyl and 24 ethyl. Furthermore the sterols composition of bees is unique across different life stages (eggs to queen) with different sterols showing greater prevalence at different growth stages showing potential importance of sterol diversity in diet.
Exploitation Route Commercail developoment of a bee diet for bee farmers.
Sectors Agriculture, Food and Drink,Environment

 
Description Meeting with the All Party parliamentary Group on Bees
Geographic Reach National 
Policy Influence Type Participation in a advisory committee
 
Description Pollinator Advisory Steering Group - Defra
Geographic Reach Europe 
Policy Influence Type Participation in a advisory committee
Impact Changes to land management and influencing implementation of UK gov ies to address land use change.
 
Description Darwin Inititative
Amount £290,000 (GBP)
Funding ID 21-012 
Organisation Government of the UK 
Department Department for International Development (DfID)
Sector Public
Country United Kingdom
Start 04/2015 
End 03/2018
 
Description INNOVATION FOR IMPROVED STRAWBERRY POLLINATION BY COMMERCIAL BUMBLEBEES USING CAFFEINE
Amount £224,560 (GBP)
Funding ID BB/P007589/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 05/2017 
End 04/2019
 
Description Harmful or healthy? Studying the effects of plant chemicals in nectar and pollen on bees 
Organisation Royal Holloway, University of London
Country United Kingdom 
Sector Academic/University 
PI Contribution Co authored proposal to Peter Sowerby Foundation
Collaborator Contribution Co authored proposal to Peter Sowerby Foundation
Impact None
Start Year 2015
 
Description Improved soft fruit pollination by bumblebees with caffeine BB/P007589/1 IPA Grant Awarded December 2016 Starts April 1st 2017 
Organisation National Institute of Agronomy and Botany (NIAB)
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution PI with University of Greenwich
Collaborator Contribution Co-I (co authors and research collaborators).
Impact None yet from the specific collaboration around improving pollination in strawberry because the project hasn;t started yet.
Start Year 2014
 
Description Improved soft fruit pollination by bumblebees with caffeine BB/P007589/1 IPA Grant Awarded December 2016 Starts April 1st 2017 
Organisation University of Greenwich
Department Department of Pharmaceutical, Chemical & Environmental Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution PI with University of Greenwich
Collaborator Contribution Co-I (co authors and research collaborators).
Impact None yet from the specific collaboration around improving pollination in strawberry because the project hasn;t started yet.
Start Year 2014
 
Description The macronutrient regulation of adult worker honeybees 
Organisation Newcastle University
Department Institute of Neuroscience
Country United Kingdom 
Sector Academic/University 
PI Contribution Co-PI investigating the key nutritional components in honeybee natural diets for the development of a food supplement for commercial bees. Natural Products chemistry of pollen and nectar.
Collaborator Contribution PI of the BBSRC funded project BB/P005276/1 The macronutrient regulation of adult worker honeybees. Conducting bioassays.
Impact Egan, P.A., Stevenson, P.C., Wright, G.A., Boylan, F, Stout, J.C. (2016) Toxic nectar varies at multiple spatial scales and in response to plant invasion. Journal of Ecology. 104, 1106-1115 Tiedeken E-J., Egan, P.A., Stevenson, P.C., Wright, G.A., Brown, M.J.F., Power, E.F., Farrell., I., Matthews, S.M., Stout, J.C. (2016) Nectar chemistry modulates the impact of invasive plant species on native pollinators. Functional Ecology. 30, 885-893. Arnold, S.E.J., Stevenson, P.C. and Belmain, S.R. (2015) Responses to colour and host odour cues in three cereal pest species, in the context of ecology and control. Bulletin of Entomological Research, 105, 417-425. Oliver, C., Softley, S., Williamson, S., Stevenson P. C.; Wright, G.A. (2015) Sodium channel activators have subtle effects on the motor function, grooming and wing fanning behaviour of honeybees (Apis mellifera). PLoS One. 10, e0133733. Mkenda P.A., Stevenson, P.C., Ndakidemi, P., Farman, D.I. and Belmain, S.R. (2015) Contact and fumigant toxicity of five pesticidal plants against Callosobruchus maculatus in stored cowpea (Vigna unguiculata). International Journal of Tropical Pest Management, 35, 172-184. Mkenda, P., Mwanauta, R., Stevenson, P.C. Ndakidemi, P., Mtei, K., and Belmain, S.R. (2015) Field margin weeds provide economically viable and environmentally benign pest control compared to synthetic pesticides, PLoS One. 10, e0143530 Wright, G.A., S. Shafir, S. W. Nicolson, P. C. Stevenson. UK Priority Patent no. P030809GB. A pollen substitute for bees. Filed 16 Nov 2015. Teideken, E-J, Stout, J.C, Egan, P., Stevenson, P.C., Wright G.A. (2014) Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. The Journal of Experimental Biology. 217, 1620-1635. Arnold S.E.J. Peralta Idrovo, M.E., Lomas Arias, L.J., Belmain, S.R., Stevenson, P.C. (2014). Herbivore Defence Compounds Occur in Pollen and Reduce Bumblebee Colony Fitness. Journal of Chemical Ecology. 40 (8), 878-881. D. Marlin, S. W. Nicolson, A.A. Yusuf, P.C. Stevenson, H.M. Heyman, K. Krüger (2014). The only African wild tobacco, Nicotiana africana: alkaloid content and the effect of herbivory, PLoS One, 9 (7), e102661. Hurst, V., Stevenson P.C., Wright,G.A. (2014). Toxic compounds induce characteristic malaise behaviours in the honeybee. Journal of Comparative Physiology A: 200 (10), 881-890.  Wright, G. A., Baker, D., Palmer, M. J., Stabler, D., Mustard, J.D., Power, E., Borland, A. M., and Stevenson, P. C. (2013) Caffeine in floral nectar enhances a pollinator's memory of reward. Science, 339: 1202-1204. Vanbergen, AJ, Baude, M., Biesmeijer, J.C., Britton, N.F., Brown, M.J.F., Brown, M., Bryden, J., Budge, G.E., Bull, J.C., Carvell, C.C., Challinor, A.J., Connolly, C.N., Evans, D.J., Feil, E.J., Garratt, M.P., Greco,M.K., Heard, M.S., Jansen, V.A.A., Keeling, M.J., Kunin W.E., Marris, G.C. Memmott, J., Murray, J.T., Nicolson,S.W., Osborne, J.L., Paxton, R.J., Pirk, C.W.W., Polce, C., Potts, S.G., Priest, N.K., Raine, N.E., Rushton, S.P., Ryabov, E.V., Shafir, S. Shirley, M.D.F., Simpson, S.J., Smart, S.M., Stevenson, P.C., Stone, G.N., Termansen, M., Wright, G.A., (2013) Threats to an ecosystem service: multifactorial pressures on insect pollinators. Frontiers in Ecology and the Environment, 11 (5): 251-259.
Start Year 2007
 
Description The role of Floral Secondary compounds in bee performance disease transmission in a natural ecosystem 
Organisation University of Massachusetts
Country United States 
Sector Academic/University 
PI Contribution Proposal submitted to National Science Foundation for 500K USD. Co written by me.
Collaborator Contribution Proposal submitted to National Science Foundation for 500K USD. Co written by me.
Impact Palmer-Young, E.; Farrell, I.W.; Adler, L.S; Milano, N., Egan, P; Irwin, R; Stevenson, P.C., 2019. Secondary metabolites of nectar and pollen: a data resource for ecological and evolutionary studies" Ecology (in press)Palmer-Young, E., Egan, P., Farrell, I., Adler, L.S., Irwin, R.E., Stevenson, P.C. 2019 Chemistry of floral rewards: intra- and interspecific variability of nectar and pollen secondary metabolites across taxa, Ecological Monographs, 89, e01335 Rothchild, K.W., Adler, L.S., Irwin, R.E., Sadd, B.M., Stevenson, P.C., Palmer-Young, E.C. (2018) Effects of short-term exposure to naturally occurring thymol concentrations on transmission of a bumble bee parasite. Ecological Entomology, 43, 567-577. Egan, P., Adler, L.S., Irwin, R.E., Farrel, I.W., Palmer-young, E., Stevenson P.C. 2018. Crop Domestication Alters Floral Reward Chemistry with Potential Consequences for Pollinator Health Frontiers in Plant Science. 9, 1357. Adler, L.S., Ellner, S.P., McArt, S.H., Stevenson, P.C., Irwin, R.E. 2018 Diseases where you dine: Plant species and floral traits associated with pathogen transmission in bumble bees. Ecology, 99, 2535-2545
Start Year 2013
 
Title Bee Nutrition 
Description Development of a complete food supplement for honeybees 
IP Reference 2016/053573 
Protection Patent application published
Year Protection Granted 2017
Licensed No
Impact N/A
 
Description Bees Needs Week outreach event in Carnaby Street with Defra 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Supporters
Results and Impact Outreach activity for Defras bees needs week showcasing UKRI funded work on nectar and pollen chemistry and pollaintor health.
Year(s) Of Engagement Activity 2018
 
Description European Research Night at Natural History Museum 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Controbution to NHM european research night talking about UKRI funded work on nectar chemistry and pollaintor health.
Year(s) Of Engagement Activity 2018
 
Description Interview with NBC News 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact INterview with NBC News for broadcast on US TV
Year(s) Of Engagement Activity 2016
 
Description Kew Science festival 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Open day with display of pollinator oriented research and activities from Kew Gardens to draw attention to the challenges facing pollinators and the research being undertaken by Kew to address pollinator declines. Also drawing attention to pollaintor diversity
Year(s) Of Engagement Activity 2018
URL https://www.kew.org/about-our-organisation/press-media/press-releases/press-release-kew-science-fest...
 
Description Pollinator Outreach Day 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Supporters
Results and Impact Open day with display of pollinator oriented research and activities in collaboration with Reading University to draw attention to the challenges facing pollinators and the research being undertaken by Kew and Reading to address pollinator declines.
Year(s) Of Engagement Activity 2016
 
Description Pollinator Outreach Day 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Open day with display of pollinator oriented research and activities in collaboration with Reading University to draw attention to the challenges facing pollinators and the research being undertaken by Kew and Reading to address pollinator declines.
Year(s) Of Engagement Activity 2017
URL https://www.youtube.com/watch?v=7HM4dQuaMSs
 
Description Royal Society Panel debate about Science Matters 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Formal debat with Professor Brian Cox host and the Royal Society infront of >1000 paying guests in Manchetser to debate the issues around food production and the impoortance of ecosystems services.
Year(s) Of Engagement Activity 2016
URL https://royalsociety.org/science-events-and-lectures/2016/12/science-matters-feeding-the-future/
 
Description Talk To Autralian National Radio 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact INterview wqith Professor Tim Entwistle for national public radio in Australia about Kew work on polliantors and the Hive.
Year(s) Of Engagement Activity 2017