The loss of pollinators is already impacting health on a scale with other global health risk factors


Inadequate pollination has led to a 3-5% loss of fruit, vegetable, and nut production and an estimated 427,000 excess deaths annually from lost healthy food consumption and associated diseases, including heart disease, stroke, diabetes, and certain cancers, according to research led by Harvard T.H. Chan School of Public Health. It is the first study to quantify the human health toll of insufficient wild (animal) pollinators on human health.

“A critical missing piece in the biodiversity discussion has been a lack of direct linkages to human health. This research establishes that loss of pollinators is already impacting health on a scale with other global health risk factors, such as prostate cancer or substance use disorders,” said Samuel Myers, principal research scientist, planetary health, Department of Environmental Health and senior author of the study.

The study will be published December 14, 2022 in Environmental Health Perspectives.

Increasing human pressure on natural systems is causing alarming losses in biodiversity, the topic of the COP 15 UN Biodiversity Conference currently taking place in Montreal. This includes 1-2% annual declines of insect populations, leading some to warn of an impending “insect apocalypse” in the coming decades.

Key among insect species are pollinators, which increase yields of three-fourths of crop varieties and are critical to growing healthy foods like fruits, vegetables, and nuts. Changes in land-use, use of harmful pesticides, and advancing climate change threaten wild pollinators, imperiling human supply of healthy foods.

The researchers used a model framework, which included empirical evidence from a network of hundreds of experimental farms across Asia, Africa, Europe and Latin America, that looked at “pollinator yield gaps” for the most important pollinator-dependent crops, to show how much crop loss was due to insufficient pollination.

They then used a global risk-disease model to estimate the health impacts the changes in pollination could have on dietary risks and mortality by country. Additionally, they calculated the loss of economic value from lost pollination in three case study countries.

The results showed that lost food production was concentrated in lower-income countries but that the health burden was greater in middle- and higher-income countries, where rates of non-communicable diseases are higher. The geographic distribution was somewhat unusual in that generally the health effects from global environmental change are centered among the poorest populations in regions such as South Asia and Sub-Saharan Africa. Here, middle-income countries with large populations – China, India, Indonesia, and Russia—suffered the greatest burden.

The analysis also showed that lower-income countries lost significant agricultural income due to insufficient pollination and lower yields, potentially 10-30% of total agricultural value.

“The results might seem surprising, but they reflect the complex dynamics of factors behind food systems and human populations around the world. Only with this type of interdisciplinary modeling can we get a better fix on the magnitude and impact of the problem,” said co-author Timothy Sulser, senior scientist, International Food Policy Research Institute.

Strategies to protect wild pollinators are not just an environmental issue, but a health and economic one as well. “This study shows that doing too little to help pollinators does not just harm nature, but human health as well,” said lead author Matthew Smith, research scientist, Department of Environmental Health.

Pollinator health has traditionally been approached by focusing on the individual, or by using a hierarchical and reductionist approach, working from internal processes through to the health of the population or species. For example, López-Uribe et al. [19, p. 271] focused on honeybees, and defined health as ‘the state of well-being that translates into the ability of organisms to acquire, allocate and use energy optimally to increase fitness’.

De Miranda et al. [20] took this further by applying a One Health perspective to a range of pollinating bees, generating a practical working definition of bee health, which enabled them to identify a set of potential metrics for identifying bee health in the field. In parallel, Parreño et al. [17] have recognized that pollinator health is influenced by multiple biological processes and environmental factors, and highlight the importance of nutritional niche space to pollinator health in the context of wild species of bees. However, such hierarchical reductionist approaches may miss key traits of pollinator health at the community level.

Here we expand on López-Uribe et al. [19] and propose an ecosystems-level approach, starting at the level of the pollinator community and its provision of pollination services (figure 1). From this perspective, pollinator health can be argued to be analogous to the stability, robustness or resilience of the pollinator community to environmental change.

Network metrics can be used to assess the health of a community [21], as can simple measures of abundance, richness and diversity. Arguably, a trait-based approach, where similar species can be considered as functional replacements, might be useful in this perspective. Thus, health at the community level might not be impacted by the loss or reduction of one species (ill-health) if it is naturally replaced by a functionally similar species.

Concomitant with this, factors such as pathogens that, at the level of individuals, might be considered as detrimental to health, could play important positive roles at the community level in maintaining species diversity, and thus community health [22]. Consequently, factors that have been previously viewed solely through the lens of pollinator health at the individual or population level, such as food availability, food quality, parasites, pathogens, and secondary chemicals that enable medication, need to be reconsidered at the pollinator community level. A definition of pollinator health at this level might mean that a healthy pollinator community is resilient in the face of environmental perturbations and provides a robust pollination service.

Figure 1.
Natural processes and anthropogenic drivers influencing pollinator health and potential mitigating solutions at community, population, social group and individual levels expanded from López-Uribe et al. [19]. (Online version in colour.)

Of course, such an ecosystem-led view does not mean that we can simply ignore the impact of environmental factors on the health of individual pollinators. Robustness and resilience at the ecosystem level need to be supported by health at the individual level, even if that does not mean equal health for every individual within every species, and so understanding how factors such as nutritional quality drive individual health, and, ultimately, reproduction, remains key. For pollinator communities to be stable in the long term, their individual components need to be healthy enough to reproduce and contribute to the next generation. Indeed, most papers in this special issue examine health at the level of individuals, with only a few focusing on the community level. We believe that incorporating a community definition of pollinator health that integrates health at the level of individuals, colonies, and populations within communities provides the path toward maintaining wild pollinator communities and the critical services they provide into the future.

    Secondary metabolites have been reported frequently in nectar and pollen [23–26], although there are surprisingly few examples reporting their effects on pollinator behaviour and health [13,24]. This may reflect challenges historically in instrumentation and analysis of compounds only available from very small sample sizes in low concentrations. Modern and highly sensitive instruments such as liquid chromatography–mass spectroscopy (LC-MS) have opened up this field.

Most compounds occurring in nectar and pollen are also recorded elsewhere in the plant [27], where many also provide a defensive function against antagonists; thus their presence in the floral reward for pollinators is a paradox [28]. For example, the insecticidal diterpene grayantoxin 1 is a defence compound against thrips in the foliage of Rhododendron simsii [29]. The same compound occurs in Rhododendron nectar at concentrations that are toxic to honeybees and mining bees whereas, conversely, bumblebees are unaffected [30]. This differential toxicity alludes to a chemical-based specialist pollinator syndrome. If consumed, these compounds could present a health challenge to bees at individual and colony levels, but for bumblebees the flowers may provide a surfeit of food since few other flower visitors can tolerate the toxins. In Ireland, the number of Bombus pascuorum nests in the vicinity of R. ponticum is almost double the number recorded elsewhere [31]. Whether this presents an adaptation by the plant to optimize pollination service or adaptation by bees to the toxin is not clear. However, invasive populations of R. ponticum in the British Isles show reduced toxin levels, suggesting that plants have modified their chemistry in response to an otherwise poorly adapted pollinator community [32]. Honeybees avoid grayanotoxin given a choice, so it does not present an individual or higher ecological tier health risk unless there are no alternative food sources. However, Egan et al. [33] report that pollinators impose negative directional selection against grayanotoxin in nectar of invasive R. ponticum, which contrasts with selection patterns quantified in the species’ native range, where this compound was under positive selection in nectar. Nectar concentrations were decoupled from those of leaves in the invasive but not the native range, which is likely to assist this species to evolve and facilitate visits by pollinators while simultaneously maintaining anti-herbivore defence.

Secondary metabolites may therefore have multiple functions for plants and drive interactions with mutualists and antagonists. This has been illustrated with caffeine, a widely distributed plant alkaloid that reportedly provides a defensive mechanism against insects through toxicity or feeding inhibition [34–36], behaviour-modifying effects at individual [37,38] and colony levels [39], as well as anti-parasite activity against microsporidian parasites of bees (Nosema spp.) [40,41]. Indeed, the bioactivity of nectar compounds against bee pathogens illustrates the most direct pollinator health impact of floral chemistry at the individual level. Compounds reported to occur in nectar or honey were evaluated against the gut parasite Crithidia bombi and shown to have antimicrobial activity, suggesting potential to mitigate the challenge of excessive disease burden [12]. More recently, acquisition of C. bombi by Bombus terrestris was shown to be significantly reduced in bees feeding on the Calluna vulgaris (ling heather) nectar metabolite, callunene [11]. Since B. terrestris feeds on heather nectar naturally, and nectar from this species is the third most abundant in the UK [16], this provided the first example of an ecologically relevant and widely available disease-mitigating benefit to pollinator health. However, callunene was not recorded in the hindgut, where parasites are most abundant, suggesting it had been metabolized, and consequently that established infections were not affected when this compound was consumed by a Crithidia-infected bee. Koch et al. [42] provide a possible explanation for this through a study of the interaction of B. terrestris with nectar compounds from lime (linden) tree flowers (Tilia spp.) and strawberry trees (Arbutus unedo). Unedone from A. unedo nectar was inhibitory to C. bombi in vitro and in B. terrestris gynes, whereas tiliaside in Tilia nectar was only inhibitory in vivo. This is because tiliaside was deglycosylated by the bumblebee during gut passage, increasing its antimicrobial activity in the hindgut, the site of C. bombi infections. Conversely, unedone was inactivated by glycosylation in the midgut by the bumblebee, only to be deglycosylated by the microbiome in the hindgut, restoring its activity. Koch et al. [42] thus demonstrate that metabolism of nectar compounds by the host or the microbiome modifies their antiparasitic activity.

When pollinators use floral resources but their larval stages feed on the foliage of the same plant, there is an ecological conflict and a challenge for the plant to mediate these interactions. Balbuena et al. [43] present one such example in Hyles lineata, a common hawkmoth that feeds on the flowers of Oenothera harringtonii whereas the larvae feed on its leaves. They monitored growth, survival and fecundity as individual-level measures of pollinator health and showed that the plant modifies floral and foliar chemistry to optimize the services of pollinators while protecting against herbivory using a complex of constitutive and induced chemical processes. The larvae of H. lineata, however, perform well on other related species of Oenothera, suggesting that in asymmetric plant–pollinator interactions alternative larval host plants are critical in maintaining pollinator health.

Mammal pollination systems have evolved in several plant families, and while some research has identified drivers of interactions between flowers and bat pollinators [44,45], there are substantial gaps in our knowledge. One outstanding question is whether sensory bias evolved to facilitate intraspecific communication or for seeking food. There are several examples of ground-dwelling mammal pollination systems in southern Africa, many of the pollinators being nocturnal and so reliant on scent. The quantities of nectar produced by the host species for mammalian pollinators are typically far greater than those provided by insect-pollinated species, so adapted to suit a specific dietary requirement. These plants flower in winter when other food for rodents is scarce. To ensure the mammalian pollinator is healthy and able to continue to provide pollination services, the floral cues provided by the flowers to attract the pollinator are critical in enabling these pollinators to find the right food. Johnson & Govender [46] report that four species of rodents were broadly attracted to oxygenated aliphatic nectar chemicals such as esters and ketones but not to aromatics (conjugated planar rings such as benzyls) which occur frequently in the floral odour of insect-pollinated plants, nor to a sulfide compound that is attractive to bats. The attractiveness of some of the ketones and esters was lost when combined with unattractive compounds, suggesting the overall chemical environment is important. These volatile floral chemicals facilitate the exploitation of rodent sensory bias that likely evolved in intraspecific communication or searching for seeds.

    Poor nutrition results from the loss of natural habitat and from extensive monoculture plantings, and diminishing forage is understood to be a major cause of pollinator declines [7–9]. Good nutrition, however, can offset stresses from pesticides and diseases. Overall, diverse and continuously available forage leads to more balanced nutrition and access to beneficial phytochemicals.

Nectar is an energy source for most pollinators. Nicolson [47] provides a broad synthesis of nectar chemistry and nutritional quality, including implications for vertebrate pollinators as well as bees. The historical context of research on nectar chemistry is touched on, but also recent metabolomic studies (e.g. [48]). A model of the mechanisms of nectar secretion [49] offers a simple explanation for the differences in nectar volume and sugar composition which have stimulated much research on the association between sucrose proportion in nectar and pollinator type. These patterns are particularly clear for nectar-feeding birds and their flowers. Apart from direct nutritional benefits, many nectar compounds such as amino acids and secondary compounds have indirect effects on foraging behaviour and parasite infection. Water, usually ignored in the composition of nectar, is also a nutrient, and the water component of nectar is a major factor in its variability but also important for consumers. Phenotypic variation in nectar chemistry is common [50], and there is increasing evidence for effects of microbial contamination on nectar chemistry [51].

Pollen is more difficult to analyse. It varies widely in nutrient composition [52,53], but much of this variation may be due to discrepancies between the methods used in pollen analysis. Differences in methods make it difficult to compare studies. In this issue, Lau et al. [54] review the common methods used to analyse pollen protein and lipids—the macronutrients most often linked to bee health. Using Brassica and Rosa pollens, they compared a subset of these methods while also carrying out a more complete analysis. Pollen has unique physical properties and it is demonstrated here that fracturing pollen grains can lead to marked increases in estimates of protein and lipid content. Fracturing may be particularly necessary for complete extraction of components such as fatty acids, which are critical for pollinator fitness [55]. Fortunately, the widely used Dumas combustion assay for nitrogen (protein) does not require this. The authors recommend the use of standardized methods to facilitate comparisons between independent studies. In addition, disrupting pollen grains before analysis, while more important for some pollens than others, may greatly reduce the variation in data on nutrient content.

The analysis of Brassica and Rosa pollens [54] included major elements: this area of pollinator nutrition is receiving increased attention and may be important for the health of honeybee colonies [56]. De Sousa et al. [57] tested the dose-related responses of young worker honeybees in cages to mineral-laced sucrose solutions. They selected the minerals most prevalent in pollen, the major source of micronutrients for bees; it is easier to study responses to minerals in solution. They divide the eight minerals tested into salts and metals: however, all are metal ions that play essential roles in insect physiology, especially transport processes and enzymatic activity [58]. Honeybees showed some regulatory ability and avoided high and potentially toxic concentrations of all minerals used except Na: this is in agreement with Bertrand’s rule, which predicts that low concentrations of micronutrients will be attractive and high concentrations will be repellent. Honeybees also obtain minerals from nectar and water [59]. Sodium is scarce in the diets of herbivores, and enriching floral nectar with sodium attracts more pollinator visits and more species [60].

The larval diets of solitary bees are a mixture of pollen and nectar with added microbes. Leonhardt et al. [61] investigated the amino acid and fatty acid profiles of pollen provisions in the solitary megachilid bee Osmia bicornis, and whether these nutrients are correlated with bacterial microbiomes in the bees and their provisions. Bee larvae and pupae and larval provisions were sampled from different populations using trap nests at sites differing in land use and thus floral resources. Pollen types in provisions were identified and the nutrients analysed. Bacterial communities of pollen provisions and bee guts showed strong overlap. Pollen-derived bacteria may play an important role in amino acid and fatty acid provisioning; on the other hand, amino acids and fatty acids in the pollen provisions may favour particular microbial communities. The authors use neural network analysis to show correlations between amino and fatty acids and bacterial genera, but it is not possible to say whether specific nutrients were synthesized by plants or bacteria (or both). Microbial interactions may explain why larvae of both specialist and generalist bees often fail to develop on unsuitable pollen diets [62].

The final paper in this section looks beyond bees to include other insect pollinator taxa and addresses pollination at the landscape scale. Jones & Rader [63] broadly review the nutritional challenges for pollinators in agroecosystems, emphasizing the need to maximize not only bee diversity and abundance but also crop pollination outcomes. Preserving remnant habitat and introducing extra floral resources do not necessarily improve pollinator health or crop yields. The challenge is that much more information is needed on the nutritional needs of specific pollinator taxa and the resources that provide them. Even for bees, most of the available information on nutritional ecology is for a limited number of species: Apis mellifera, Bombus and mason bees (Osmia) [64]. Traditional and new approaches to evaluating nutritional requirements are outlined here and by [65]. Some of these methods can be applied to non-bee taxa. There is also a compelling need to redress the geographical bias in crop pollination studies [66].

    Microorganisms are major drivers of pollinator health. On the scale of the individual, effects of microbial associates on host health form a continuum from the negative impacts of parasites to benefits derived from symbionts, and can change on ecological or evolutionary time scales [67].

While parasites of pollinators can reduce individual health parameters such as reproductive capacity, foraging ability and physiological state, hosts can reduce negative effects of parasites through the action of their immune system, or through specific diets with medical antiparasitic effects. A better understanding of the natural mechanisms by which pollinators are able to prevent, reduce or tolerate parasite infections may inform pollinator conservation decisions, if they are, for example, linked to the availability of certain nectar or pollen sources in the environment [68]. Certain diets can reduce parasite infections in pollinators, for example through the antiparasitic activity of nectar secondary metabolites ([42]; see discussion above). Direct chemical effects of specific diets on parasites may, however, not be the only mechanisms of antiparasitic action. A sunflower pollen diet has, recently, been shown to induce strong and consistent reduction in the infections of bumblebees with the gut parasite C. bombi [69], but, so far, chemical constituents of sunflower pollen have not been shown to induce this effect [70]. In this special issue, Fowler et al. [71] test if the antiparasitic effect of sunflower pollen could instead derive from a modulation of the immune response of bumblebees. Bumblebees feeding on a sunflower or wildflower control diet did not differ in their induced or constitutive immune responses as measured by the activity of phenoloxidase and the humoral antibacterial activity of haemolymph. This suggests that the antiparasitic effects of a sunflower pollen diet are either linked to immune parameters (although these were not measured), or derive from a different, as yet unknown mechanism.

Beneficial microbial symbionts of pollinators can improve pollinator health through digesting or detoxifying diet components, defending against parasites, or stimulating immune and metabolic pathways of the host. Motta et al. [72] review the existing literature on these health benefits derived from the bacterial microbiome of social corbiculate bees (honeybees, bumblebees, stingless bees), and present new data on the potential of inoculating honeybees with probiotic bacteria as a way to improve their health. They highlight that stressors like antibiotics or poor diet may disrupt the bee microbiome, and lead to increased disease susceptibility. Administering probiotic bacteria to bees has the potential to restore health-promoting microbiomes, but experimental evidence for the promise of this approach is largely missing. Motta et al. [72] experimentally show that commercially available probiotics with bacteria that are not natively found in the honeybee gut fail to colonize honeybees, while cultured native bacterial strain colonies efficiently and induce the activation of immune and metabolism genes. This suggests existing probiotics may have limited or no benefits for honeybees, but future probiotic research in bees should focus on using bacterial strains with beneficial health effects naturally found in bees.

Martin et al. [51] looked beyond the endogenous gut microorganisms of pollinators, and review the potential effects of nectar microbes on pollinator health. Bacteria and yeasts in nectar alter its chemical composition, with negative (e.g. reduced sugar content) or positive (e.g. increased amino acid content, increased amounts of micronutrients like vitamins and sterols) effects for pollinator nutrition and health. Pollinators may modulate their foraging behaviour based on microbial presence in nectar, likely through detecting volatile organic compounds released by nectar microbes. This may facilitate the detection of nectar sources for pollinators and may affect pollination services on a landscape scale. Martin et al. [51] also argue for more research into the effects of nectar microbes on disease dynamics in pollinators, as these microorganisms could affect floral transmission of pollinator pathogens, or infections within pollinators, for example through the production of antibiotic compounds by floral yeasts.

Nicholls et al. [73] highlight the importance of foraging behaviour for disease dynamics of pollinators. Horizontal transmission of pollinator pathogens often occurs on flowers [74,75]. A better understanding of the factors affecting floral pollinator disease transmission, such as floral traits and effects of flowering plant species diversity, may inform a better design of managed landscapes to reduce the spread of pollinator diseases. Existing studies in part show contradictory patterns for this interaction [73], but investigating effects of different foraging behaviour of diverse pollinator species on disease transmission may help resolve this.

Brown [22] provides an important community- and landscape-level view of pollinator health, which argues for considering pollinator parasites as an integral part of biodiversity. While most research on pollinator health has focused on the detrimental effects of parasites on individual or colony host health, at a landscape level, parasites may facilitate coexistence of diverse pollinator communities, and are major natural drivers of evolutionary dynamics. Therefore, Brown [22] argues that natural host–parasite interaction networks should be conserved, rather than eliminated. A better understanding of the impacts of floral rewards on host–parasite interactions may be used to design landscapes that support pollinators to moderate levels of parasite infections and ensure pollination services.

reference link :

More information: Pollinator deficits, food consumption, and consequences for human health: a modeling study, Environmental Health Perspectives (2022). DOI: 10.1289/EHP10947


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