Buzzkill: Pollinators and Food Security

For approximately 75% of all flowering plants on the planet, comprising over 250,000 species. sexual reproduction is dependent upon an animal partner for assistance with pollination—the movement of pollen grains, produced by anthers, to receptive female stigmatic surfaces. The number of animal species involved in pollination has been estimated at upwards of 150,000, the vast majority of which (>99%) are insects. Recent declines in populations of pollinators of all stripes, as it were, have rightly raised concerns about global food security (National Academy of Sciences 2007). Pollinators contributed an estimated $170 billion (€150 billion) to global agricultural food production in 2005, amounting to almost 10% of total global agricultural production for direct human consumption (Gallai et al. 2009). Although the bulk of calories consumed by humans derive from wind-pollinated grains such as rice, wheat, and corn, insect pollination in particular is disproportionately important in global production of fruits, vegetables, edible oil crops, stimulant crops, and nuts.  Moreover, global production of crops pollinated by insects has increased dramatically over the past half-century, tripling the demand for agricultural pollination services (Aizen and Harder 2009) and raising the specter of critical shortages in the foreseeable future.
It is no easy task to estimate the value of pollination services to agriculture or to predict their role in food security (Melathopoulos et al. 2015); any such effort is seriously hampered by yawning data chasms relating to the size and distribution of pollinator populations and to the relative magnitude of the contribution of any specific species to productivity of any specific crop in any specific locality. A much quoted figure is that one species, Apis mellifera, the western honey bee, is directly or indirectly responsible for production of over 90 crops in the U.S. alone, which collectively amount to approximately one-third of the American diet. Certain unique biological attributes contribute to the status of honey bees as premier managed pollinator not just in the U.S. but throughout the world: large perennial colonies with tens of thousands of workers that can forage effectively for nectar and pollen across U.S. monocultures, a generalized diet that allows honey bees to utilize a tremendously broad variety of plant species, communication behavior that can direct foragers to particular locations and increase the likelihood of cross-fertilization, and a predilection for nesting in cavities and their wooden box surrogates, which makes honey bees readily transportable. Thus, in the U.S., managed pollination services provided by honey bees across the agricultural spectrum has been valued in excess of $15 billion (NAS 2007). The relative importance of managed pollination varies both quantitatively and qualitatively by crop; honey bees are, for example, responsible for pollinating 100% of almonds and 90% or more of apple, sunflowers, and sweet cherries (Morse and Calderone 2000). Among vegetables, 90% or more of commercial production of asparagus, avocado, broccoli, carrot, cauliflower, celery, cucumber, onion, and pumpkin depends on bees. Honey bees indirectly benefit the beef and dairy industry by virtue of contributing the bulk of pollination services for producing alfalfa and clover, the main sources for cattle fodder, and the value of crops that do not even absolutely require insect pollinators for seed production, including soybeans, olives and grapes, can be enhanced by bee visitation, which can improve yields and quality. Potts et al. (2010) calculated that a loss of honey bee pollination services would translate into a production deficit of 6% for vegetables and 12% for fruits in the context of current consumption levels —and, due to changing values and dietary practices, acreages planted in fruits and vegetables worldwide have been steadily increasing worldwide, presaging a potential future of shortages and escalating prices.
That data chasms exist with respect to pollinator identity, efficacy, distribution and abundance is a reflection of a long history of ignorance and/or indifference, willful or otherwise, arising from the erroneous assumption that pollination services constitute an inexhaustible natural resource, not unlike sunlight.  The National Agricultural Statistics Survey (NASS) began to record numbers of honey-producing colonies of honey bees in 1947; this systematic survey recorded a 60% decline in the number of colonies between 1947 and 2005 (NAS 2007). In late fall 2006 and continuing through 2007, sudden massive inexplicable losses among managed honey bee populations, ultimately associated with a distinct syndrome dubbed Colony Collapse Disorder, created acute shortages and dramatically increased rental fees for honey bees, particularly among almond growers, who at that time required the use of approximately half of all American colonies (circa 1.2 million) to meet the pollination needs of over 600,000 acres of almond trees at flowering. The demand for pollination from just one commodity group (albeit one that at the time was worth $2.5 billion) brought into sharp focus the need for better data on managed pollinator stocks. Since that time, consistent standardized annual surveys by the Bee Informed Partnership, a nationwide collaboration aimed at documenting and understanding colony losses, have documented steady overwintering losses ranging between 22% and 36%, well above anecdotally estimated historical levels. At least for managed honey bees, there is a historical baseline; such baseline population data are essentially nonexistent for the vast majority of pollinator species. 
            Whatever the cause or causes of Colony Collapse Disorder (which remain in dispute) and irrespective of whether it remains a distinct cause of colony losses (also in dispute), the phenomenon of CCD made abundantly clear the precarious status of American honey bees, contending with a myriad of challenges, including pathogens, parasites, pesticides, and modern management practices, all of which interact in a diversity of ways.  Linking all of the potential drivers of colony decline, though, is the fact that pollinators today are facing their own food security issues. Erosion of quality and diversity of food resources has certainly affected honey bee health on the national level and likely contributes to declines across the pollinator spectrum.  Urbanization, development and monoculture agriculture are accompanied by regional losses in plant diversity, and habitat loss not surprisingly has been linked to colony losses. In the U.S.,  Naug (2009) found that the amount of open land is directly correlated with honey yield and the ratio of open to developed land is inversely correlated with the proportion of colony losses. The problem is not limited to the U.S.; in England, the protein content of beebread, the fermented form of pollen stored in the hive and used as food for workers and larvae, was negatively corrected with landscape coverage by farmland near hives and positively correlated with landscape coverage by woodlands and natural grasslands (Donkersley et al. 2012). Other bees are similarly affected; between 1978 and 1998, for example, over three-quarters of plant species visited by bumble bees declined in frequency (Potts et al. 2010). Beyond changes in land use, extreme weather events, particularly drought, can exacerbate losses in floral diversity; in fact, heavy overwintering losses of honey bees in 2013 were thought to be linked to the severe summer drought across most of the country in 2012. Droughts adversely affect bee health by reducing the overall availability of nectar and pollen and increasing the need for individual foragers to fly greater distances in search of adequate food resources. Periods of extreme heat (and extreme cold) can also cause major losses and in view of the fact that among the predicted consequences of global environmental change is an increasing frequency of extreme weather events (IPCC 2007), food shortages for honey bees will likely increase in frequency and intensity.
Loss of diversity is particularly problematical for Apis mellifera, the western honey bee, the world’s premier managed pollinator. The very attributes that make the western honey bee so useful also make it distinctively vulnerable.  The large perennial colonies demand enormous inputs of nectar and pollen throughout the entire growing season—from early spring through fall in temperate North America.  The nutritional physiology of the species reflects its longstanding evolutionary association with a diversity of food resources.  Honey bees have evolved to consume a diversity of food sources and a reduction in floral diversity can impede growth and development. Consuming pollen from diverse sources increases honey bee immunocompetence (Alaux et al. 2010). Larval bees consuming pollen from multiple sources of pollen exhibit superior resistance to bacterial infections and opportunistic fungi (including Aspergillus species) than those consuming pollen from a single pollen source (Foley et al. 2012), and a diet of pollen from multiple species of plants improves the ability of bees to fend off Nosema ceranae, a devastating microsporidial pathogen, than a diet consisting of a single pollen type (DiPasquale et al. 2010).
Habitat loss due to landscape-scale conversion has long been a concern in pollinator conservation but the rates of habitat loss have been increasing due to changes in the economic and political landscape. In the U.S., the Conservation Reserve Program provides incentives for farmers to use low-quality land (e.g., prone to erosion or flooding) for planting environmentally beneficial vegetative cover, including, among others, pollinator habitat. In 2013, the total acreage enrolled, 25.3 million acres, was the lowest total since 1988 when the program had just started. In the Midwest U.S., much of the land in the conservation reserve program was taken out in order to plant corn for use as a biofuel feedstock, decreasing diversity in an already depauperate landscape (in Illinois, the “Prairie State,” less than 0.01% of native tallgrass prairie remains undisturbed; in 2013, >80,000 acres were taken out of CRP).  Landscape scale biofuel feedstock conversion had an additional impact on pollinators in that, in the Corn Belt (IA, IL, IN, MO, OH), much of the corn acreage expansion came at the expense of soybean acreage (http://www.ers.usda.gov/amber-waves/2011-september/data-feature-where-did-the-corn-come-from.aspx#.VLE6ISfZcSA); unlike wind-pollinated corn, soybeans provide both nectar and pollen for pollinators. Over the 2012-2013 season, among the leading causes of colony failure reported by beekeepers in backyard or sideline operations was starvation (Steinhauer et al. 2014).
Imminent starvation has other impacts on the health of honey bee colonies in that, in the absence of adequate natural forage, beekeepers often resort to replacing honey with sucrose or high fructose corn syrup. These food substitutes have subtle effects on health that, in hindsight, are not altogether surprising.  Bees consuming honey (in contrast with sucrose or high fructose corn syrup) have higher levels of expression of genes associated with both immunity and detoxification (Mao et al. 2013). Multiple phytochemicals in nectar and pollen, as well as in propolis (the glue-like material processed from plant resins that bees use to line cells and repair defects in the hive) upregulate detoxification genes and enhance metabolism of both natural and synthetic toxins. These same substances act as “nutraceuticals” and also upregulate immunity genes. In their absence, the ability of honey bees to cope with multiple forms of environmental stress can be compromised.
Beyond losses in quantity of food resources through outright habitat loss, honey bees also must cope with reductions in food quality through habitat degradation. Widespread contamination of landscapes by agricultural chemicals exacerbates the problems presented by declining floral diversity. With bodies covered with branched hairs that can carry an electrostatic charge, honey bees are built to collect, retain, and transport pollen grains, but the same morphological and behavioral attributes predispose them to collect contaminants and bring them to the hive. The extent to which agricultural landscapes are contaminated with agrochemicals is dramatically illustrated by the discovery of residues of >120 pesticides and metabolites in beehives, in wax, pollen, and the bees themselves (Mullin et al. 2010).  The most frequently encountered contaminants (detected in almost 100% of wax foundation samples) were the acaricides tau-fluvalinate and coumaphos, introduced into the hive deliberately by beekeepers desperate to control the ectoparasitic varroa mite, which kills bees directly by sucking hemolymph and which weakens colonies by acting as a vector for more than a dozen viral pathogens.  Although these two acaricides are individually safe for bees when used at therapeutic concentrations, when encountered at the same time they synergize each other—that is, each enhances the toxicity of the other.  Thus, the virtually complete contamination of wax foundation by these two pesticides renders honey bees vulnerable to pesticide toxicity even in the absence of agrochemical contaminants.
Almost as ubiquitous in the hive environment as acaricides are fungicides, widely used by farmers to cope with plant fungal diseases. Although designed to interfere with biochemical targets of fungi, fungicides can compromise bee health in a variety of (sometimes unexpected) ways. The so-called ergosterol-biosynthesis inhibiting fungicides (EBI) owe their antifungal activity due to their ability to interfere with the function of the enzyme lanosterol 14α-demethylase, an enzyme in the cytochrome P450 superfamily which regulates the biosynthesis of ergosterol.  Because animals rely on a structurally different sterol, cholesterol, and do not biosynthesize ergosterol, nontarget toxicity of the EBI fungicides was assumed to be low. Although direct toxicity may in fact be low, it has long been known that these compounds interfere broadly with other cytochrome P450 functions, including detoxification of pesticides. The honey bee genome project revealed that honey bees have a dramatically reduced inventory of detoxification genes and one consequence is that there are few cytochrome P450 monooxygenase enzymes equipped to detoxify xenobiotics (Claudianos et al. 2006).  When two potential substrates compete for access to the same catalytic site of an enzyme, neither is metabolized very efficiently and the result is synergistic enhancement of toxicity.  Prochloraz, an EBI fungicide, was shown to interfere with honey bee detoxification of pyrethroid pesticides over 20 years ago; almost every class of insecticide introduced in the intervening years (including but not limited to new pyrethroids, neonicotinoids, and fenpyroximate) is also synergized by these EBI pesticides (Glavan and Bozic 2013). Fungicide contaminants thus have the potential for rendering other residues substantially more toxic.  
            Fungicide contaminants in pollen can also render honey bees more vulnerable to their own fungal pathogens. Pettis et al. (2013) examined pollen brought back to hives by foraging bees and found high fungicide loads; moreover, bees consuming pollen heavily contaminated with fungicides were more susceptible to infection by the fungal pathogen Nosema ceranae. Two fungicides predictably found as contaminants in beehives, chlorothalonil and pyraclostrobin, were associated with a twofold to threefold higher risk of Nosema infection. In addition to fungal pathogens, bees share their environment with beneficial fungi that are potential inadvertent targets for fungicide contaminants. Honey bees do not eat substantial quantities of raw pollen; rather, pollen is processed in the hive via fermentation and converted to a storable form called beebread. Some of the fermentation is carried out by lactic acid bacteria that are found in the “honey stomach” ; these bacteria likely colonize the stored pollen via regurgitated nectar that is added to pollen during processing (Vasquez et al. 2012). Beyond the endosymbiotic microbial communities, bees also depend on fungi for processing pollen and making beebread. Over 20 years ago, Gilliam et al. (1989) identified more than 20 different species of fungi in beebread; which are symbiotic and which are environmental contaminants has not yet been determined.  What is known, though, is that bees that forage in agricultural landscapes in which multiple fungicides are used have vastly reduced fungal diversity in their hives (Yoder et al. 2010). The importance of fungal diversity to hive health is suggested by the phenomenon of “entombed pollen”—cells with pollen and beebread that are capped and never used as food. Such sells contain beebread heavily contaminated with fungicides (vanEngelsdorp et al. 2010).
Neonicotinoids are neurotoxic pesticides formulated for systemic application that, although rarely present as contaminants in hives the U.S., have nonetheless attracted the most attention from the general public as problematical for bees.  Some of the neonicotinoids (notably clothianidin and imidacloprid) are indeed highly toxic to honey bees in laboratory assays and several field studies have demonstrated sublethal effects on forager behavior and potential colony-level impacts on survivorship and reproduction. Irrespective of the exposure risks, sublethal, and lethal impacts of these systemic pesticides, what is perhaps most troubling about them, in the context of honey bee health, is not that they are used but how they are used. Neonicotinoids are widely used in conjunction with fungicides as seed treatments (notably for corn and soybean), to protect against root pests and, through systemic distribution throughout the plant, against sap-feeding pests. Bees have clearly experienced mortality through direct contact with dust during corn planting (resulting from a problem with formulation) and they can at least in theory ingest a potentially lethal amounts through contaminated nectar, pollen, and guttation water.   
            Clearly, neonicotinoid pesticides that dislodge from the seeds to which they are applied (along with fungicides) are not only environmentally a disaster for honey bees, they are in effect an economic loss to the growers, who are paying a premium for a product that does not perform as advertised. In addition, the use of systemic pesticides irrespective of whether pests are present violates long-established principles of integrated pest management, according to which pesticides are used when pest pressures reach a level at which pest control treatments are economically justifiable (i.e, provide an economic return). While estimating the economic threshold can be difficult across different crops with different pests, the concept of taking action once a pest has been detected is a venerable one, offering environmental benefits (not the least of which is reducing the risk of resistance evolution) as well as economic benefits, sparing farmers unnecessary expenses. Moreover, in 2014, the Biological and Economic Analysis Division (BEAD) of the Environmental Protection Agency conducted an analysis of the “Benefits of neonicotinoid seed treatments to soybean production” (October 2, 2014). They concluded that “these seed treatments provide negligible overall benefits to soybean production in most situations. Published data indicate that in most cases there is no difference in soybean yield when soybean seed was treated with neonicotinoids versus not receiving any insect control treatment.  Furthermore, neonicotinoid seed treatments as currently applied are only bioactive in soybean foliage for a period within the first 2-4 weeks of planting, which does not overlap with typical periods of activity for some target pests of concern” (http://1.usa.gov/1ucfY6a).
            Honey bees (and other pollinators) have enough troubles with habitat loss and degradation due to agricultural expansion to feed a hungry world; although use of insecticides and other pesticides to combat pests can be both economically and environmentally justifiable, that use should not be as an “insurance benefit against sporadic and unpredictable pests.”  While the EPA failed to find “real-world significance of this benefit”, there is increasing evidence that such practicides present real-world risks to pollinator partners, which are the best insurance Americans have for food security in the future.
 

 
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Author: Dept. Entomology University of Illinois at Urbana-Champaign

Dept. Entomology University of Illinois at Urbana-Champaign
May Berenbaum graduated summa cum laude, with a B.S. degree and honors in biology, from Yale University in 1975 and received a Ph.D. in ecology and evolutionary biology from Cornell University in 1980.