Critical links between biodiversity and health in wild bee conservation
Authors: M.A. Parreño, C. Alaux, J.-L. Brunet, L. Buydens, M. Filipiak, M. Henry, A. Keller, A.-M. Klein, M. Kuhlmann, C. Leroy, I. Meeus, E. Palmer-Young, N. Piot, F. Requier, F. Ruedenauer, G. Smagghe, P.C. Stevenson, S.D. Leonhardt
Journal: Trends in Ecology & Evolution (2021)

The diversity, abundance, and health of wild bees is jeopardized primarily by land-use modifications, among other global change drivers.Defining and measuring health in wild bees requires an integrative approach across disciplines.We use elements from chemistry, stoichiometry, ecology, physiology, pathology, and genetics to (i) contribute to a more comprehensive definition of wild bee 'health', and (ii) define a framework linking bee health with floral resource/nutritional landscapes through assessing species-specific nutritional niches.We suggest a novel and holistic approach for capturing bee health through combining field and laboratory tools.Knowledge gained by applying this framework will serve as a blueprint for stakeholders engaged in pollinator conservation. Wild bee populations are declining due to human activities, such as land use change, which strongly affect the composition and diversity of available plants and food sources. The chemical composition of food (i.e., nutrition) in turn determines the health, resilience, and fitness of bees. For pollinators, however, the term 'health' is recent and is subject to debate, as is the interaction between nutrition and wild bee health. We define bee health as a multidimensional concept in a novel integrative framework linking bee biological traits (physiology, stoichiometry, and disease) and environmental factors (floral diversity and nutritional landscapes). Linking information on tolerated nutritional niches and health in different bee species will allow us to better predict their distribution and responses to environmental change, and thus support wild pollinator conservation. Wild bee populations are declining due to human activities, such as land use change, which strongly affect the composition and diversity of available plants and food sources. The chemical composition of food (i.e., nutrition) in turn determines the health, resilience, and fitness of bees. For pollinators, however, the term 'health' is recent and is subject to debate, as is the interaction between nutrition and wild bee health. We define bee health as a multidimensional concept in a novel integrative framework linking bee biological traits (physiology, stoichiometry, and disease) and environmental factors (floral diversity and nutritional landscapes). Linking information on tolerated nutritional niches and health in different bee species will allow us to better predict their distribution and responses to environmental change, and thus support wild pollinator conservation. Bees decline because their food sources disappearAnimals pollinate >85% of flowering plants and 75% of the leading crops worldwide [1.Klein A.-M. et al.Importance of pollinators in changing landscapes for world crops.Proc. Biol. Sci. 2007; 274: 303-313Crossref PubMed Scopus (3270) Google Scholar] which provide food and medicines for other animals and humankind. 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Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES), 2016Google Scholar].Alarmingly, many wild bee populations are declining due to the impact of different biotic and abiotic stressors caused by human activities that act alone or in combination, such as pesticides, invasive species, pathogens, intensive land-use, and climate change [5.Dicks L. et al.A global assessment of drivers and risks associated with pollinator decline.Nat. Ecol. Evol. 2021; 5: 1453-1461Crossref PubMed Scopus (4) Google Scholar, 6.Eggleton P. The state of the world's insects.Annu. Rev. Environ. Resour. 2020; 45: 61-82Crossref Scopus (15) Google Scholar, 7.Rhodes C.J. Pollinator decline – an ecological calamity in the making?.Sci. Prog. 2018; 101: 121-160Crossref PubMed Scopus (36) Google Scholar, 8.Storkey J. et al.Wild pollinators in arable habitats: trends, threats and opportunities.in: Hurford C. 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The Bees of the World. Johns Hopkins University Press, 2007Google Scholar, 21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar, 22.Ziska L.H. et al.Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees.Proc. R. Soc. B Biol. Sci. 2016; 283: 20160414Crossref PubMed Google Scholar, 23.Requier F. et al.Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds.Ecol. Appl. 2015; 25: 881-890Crossref PubMed Scopus (171) Google Scholar].Nutritional landscapes of beesAs nutritional intake and thus the nutrient composition (henceforth referred to as nutritional quality) of food strongly determine the health, resilience to pathogens, and fitness of animals [24.Simpson S.J. Raubenheimer D. The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity. Princeton University Press, 2012Crossref Google Scholar], access to food resources that enable diverse and balanced nutrition is one key driver of population stability [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar]. In this context, we consider a nutrient to be any chemical compound (i.e., from chemical elements, phospholipids, and amino acids to 'group components' such as proteins) that are part of the food/nutrition of bees. Bees obtain most nutrients and several potential medically active plant secondary metabolites from flowering plants by consuming mostly nectar and pollen [20.Michener C.D. The Bees of the World. Johns Hopkins University Press, 2007Google Scholar,25.Koch H. et al.Flagellum removal by a nectar metabolite inhibits infectivity of a bumblebee parasite.Curr. Biol. 2019; 29: 3494-3500Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar,26.Stevenson P.C. For antagonists and mutualists: the paradox of insect toxic secondary metabolites in nectar and pollen.Phytochem. Rev. 2020; 19: 603-614Crossref Scopus (17) Google Scholar]. Nectar primarily provides carbohydrates for maintaining energy and metabolic processes, whereas pollen is the main source of all other macronutrients (i.e., protein and fat) and micronutrients (e.g., vitamins, sterols) that are required for tissue homeostasis, development (e.g., ovary development), and larval growth [27.Filipiak M. A better understanding of bee nutritional ecology is needed to optimize conservation strategies for wild bees – the application of ecological stoichiometry.Insects. 2018; 9: 3Crossref Scopus (16) Google Scholar, 28.Nicolson S.W. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two.Afr. Zool. 2011; 46: 197-204Crossref Google Scholar, 29.Wright G.A. et al.Nutritional physiology and ecology of honey bees.Annu. Rev. Entomol. 2018; 63: 327-344Crossref PubMed Scopus (89) Google Scholar]. Ideally, floral communities provide food resources of both sufficient quality and quantity. The quantity of food resources is determined by the abundance of flowers present in the landscape – namely the number of plants/flowers present per species and the overall amount of flowering species [30.Timberlake T.P. et al.Phenology of farmland floral resources reveals seasonal gaps in nectar availability for bumblebees.J. Appl. Ecol. 2019; 56: 1585-1596Crossref Scopus (56) Google Scholar]. The quality of food resources depends on the composition of different flowering plant species because each plant species provides pollen and/or nectar with a specific nutrient profile [31.Jachuła J. et al.Habitat heterogeneity helps to mitigate pollinator nectar sugar deficit and discontinuity in an agricultural landscape.Sci. Total Environ. 2021; 782146909Crossref PubMed Scopus (5) Google Scholar]. In fact, the nutritional profiles of pollen and nectar vary greatly among different plant species [32.Belsky J. Joshi N.K. Impact of biotic and abiotic stressors on managed and feral bees.Insects. 2019; 10: 233Crossref Scopus (37) Google Scholar, 33.Palmer-Young E.C. et al.Chemistry of floral rewards: intra- and interspecific variability of nectar and pollen secondary metabolites across taxa.Ecol. 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Floral communities, which are characterized by a specific composition and diversity of flowering plant species, consequently determine resource availability and diversity, and thus determine the nutritional landscape in which bees are foraging [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar]. More details of variation in nutritional quality in pollen and nectar, the effect of different diets on bee performance and fitness, and differences in foraging preferences among bees are given in Vaudo et al. [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar].Although much less well understood, the nutritional needs of bee species are also expected to differ substantially between bee species [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar]. The sustainability of bee populations thus depends on flowering plant communities that provide sufficient amounts of the different nutrients required because the quality of food, and in particular of pollen, directly determines offspring survival and development, and can therefore influence the entire population [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar,37.Filipiak Z.M. Filipiak M. The scarcity of specific nutrients in wild bee larval food negatively influences certain life history traits.Biology. 2020; 9: 12Crossref Scopus (6) Google Scholar,38.Moerman R. et al.Pollen nutrients better explain bumblebee colony development than pollen diversity.Insect Conserv. Divers. 2017; 10: 171-179Crossref Scopus (39) Google Scholar].Surprisingly, the interaction between flowering plant communities, the available nutritional landscape, and the health status of different wild bee species has hitherto received little attention (cf [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. Insects Vectors Med. Vet. Entomol. 2015; 10: 133-141Google Scholar,34.Vaudo A.D. et al.Pollen protein: lipid macronutrient ratios may guide broad patterns of bee species floral preferences.Insects. 2020; 11: 132Crossref Scopus (41) Google Scholar]). This knowledge is, however, crucial for determining how floral communities and respective conservation measures can support wild bee populations. We therefore propose a conceptual framework for how anthropogenic changes in flowering plant communities can affect bee communities by altering the nutritional landscape and thus niches available to support healthy wild bee populations.Measuring wild bee healthAlthough human health is understood as the physical, mental, and social well-being of an individual or population, the health of wildlife has generally been understood as the absence of disease [39.Stephen C. Toward a modernized definition of wildlife health.J. Wildl. Dis. 2014; 50: 427-430Crossref PubMed Google Scholar]. For pollinator communities, the term 'health' only recently appeared in the literature and its precise definition is still subject to debate [40.López-Uribe M.M. et al.Defining pollinator health: a holistic approach based on ecological, genetic, and physiological factors.Annu. Rev. Anim. Biosci. 2020; 8: 269-294Crossref PubMed Scopus (16) Google Scholar]. López-Uribe et al. suggested a multilevel approach and the use of various parameters to measure bee health at the individual, colony, and population level [40.López-Uribe M.M. et al.Defining pollinator health: a holistic approach based on ecological, genetic, and physiological factors.Annu. Rev. Anim. Biosci. 2020; 8: 269-294Crossref PubMed Scopus (16) Google Scholar]. The health status of a population should then be a direct consequence of the average health status of individuals, where population size is likely to correlate positively with average individual health.We propose to apply a multidimensional concept of bee health to wild bees – defined as the status of well-being of each individual as a result of their interaction with the local environment (Figure 1). We suggest that all or several of the following physiological parameters should be recorded and integrated to comprehensively capture individual bee health – the composition and amount of stored nutrients in bee bodies (such as proteins, lipids, glycogen, chemical elements), body size [41.Dellicour S. et al.Distribution and predictors of wing shape and size variability in three sister species of solitary bees.PLoS ONE. 2017; 12e0173109Crossref PubMed Scopus (18) Google Scholar], pathogen load, beneficial microbiota [42.Engel P. et al.The bee microbiome: impact on bee health and model for evolution and ecology of host–microbe interactions.mBio. 2016; 7e02164-15Crossref Scopus (130) Google Scholar], immunocompetence [43.Alaux C. et al.Diet effects on honeybee immunocompetence.Biol. Lett. 2010; 6: 562-565Crossref PubMed Scopus (454) Google Scholar], and fertility [44.Keller A. et al.(More than) Hitchhikers through the network: the shared microbiome of bees and flowers.Curr. Opin. 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For instance, diet quality correlates with increased levels of the storage protein and antioxidant vitellogenin in individual honey bees, and this in turn correlates with higher overwintering survival of the entire colony [19.Smart M. et al.Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use.PLoS ONE. 2016; 11e0152685Crossref Scopus (104) Google Scholar,47.Alaux C. et al.A 'landscape physiology' approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats.Sci. Rep. 2017; 7: 40568Crossref PubMed Scopus (57) Google Scholar]. Energy storage is crucial for bee survival. The main categories of macronutrients used for energy storage in insects (glycogen, lipids, and proteins) affect several life-history traits such as dispersal capacity, reproduction, diapause, and survival [48.Arrese E.L. Soulages J.L. Insect fat body: energy, metabolism, and regulation.Annu. 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Measurement of multiple variables can therefore provide a more complete picture of pollinator health status than focusing on a single parameter.Floral diversity as an environmental driver of bee healthFloral diversity, abundance, and community composition correlate with the abundance and diversity of wild bee species [56.Albrecht M. et al.The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis.Ecol. Lett. 2020; 23: 1488-1498Crossref PubMed Scopus (113) Google Scholar,57.Dainese M. et al.A global synthesis reveals biodiversity-mediated benefits for crop production.Sci. Adv. 2019; 5eaax0121Crossref PubMed Scopus (245) Google Scholar] through food availability [58.Kaluza B.F. et al.Social bees are fitter in more biodiverse environments.Sci. Rep. 2018; 8: 12353Crossref PubMed Scopus (36) Google Scholar], nutritional quality or content [21.Vaudo A.D. et al.Bee nutrition and floral resource restoration.Soc. 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Moreover, resource diversity increases the opportunities for specialist (oligolectic) bee species with restricted pollen host plants to find suitable food resources. In generalist (polylectic) species, access to a diverse spectrum of resources supports immunity, health, performance, and survival (Table 1), presumably through ready access to adequate nutrition and beneficial plant secondary metabolites. By contrast, chronic intake of monotonous, nonsuitable, low quality, or toxic food reduces the immune-competence and vitellogenin levels of bees, thus affecting bee health through 'nutritional stress' [47.Alaux C. et al.A 'landscape physiology' approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats.Sci. Rep. 2017; 7: 40568Crossref PubMed Scopus (57) Google Scholar,66.Brunner F.S. et al.Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris.Proc. Biol. 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Rep. 2017; 7: 40568Crossref PubMed Scopus (57) Google Scholar]Monofloral diet combined with pesticides; effects on colony performanceBuff tailed bumblebee (Bombus terrestris)Additive negative effects of monofloral diet and pesticides on colony growth, drone size, and reproduc