Due to their important role in agriculture and well-documented, ongoing losses, a great deal of research has focused on characterizing and mitigating challenges to honey bee health. Using honey bees as a model species, this article summarizes biotic and abiotic stressors of pollinators including: exposure to parasites and pesticides, poor nutrition, habitat destruction and climate change.

Varroa mite (on adult bee): Acari: Apis mellifera - Image by Maryann Frazier

Varroa mite (on adult bee): Acari: Apis mellifera - Image by Maryann Frazier

For the last 10 years, US beekeepers have reported losing approximately 30% of their colonies during each winter, with total annual colony losses sometimes reaching as high as 42% (Bee Informed Partnership). These annual losses take a heavy toll on beekeepers and threaten commercial crop production. Several factors contributing to colony losses have been identified, including exposure to parasites, contact with agricultural or beekeeper applied chemicals, poor nutrition, habitat loss and climate change.

Honey bee parasites, pathogens and pests

Honey bee (Apis mellifera) hives are busy and crowded environments. Each social colony has 1 reproductively active queen, approximately 50,000+ adult workers (the queen's daughters) and depending on the season, up to several thousand adult drones (the queen's sons) [3]. In the spring and summer, colonies also contain thousands of immature bees laid by the queen. (During peak egg-laying periods, the queen can lay up to 2,000 eggs a day!) With so many individuals packed into a close environment, diseases can travel quickly. Individual honey bees have immune systems that provide molecular defenses against infection [4]. Bees also work cooperatively to keep their colonies healthy [5]. For example, workers groom each other and remove dead bees from their colony to prevent disease outbreaks.

Despite numerous physiological and behavioral defenses, honey bees are plagued by viral, fungal and bacterial infection. Furthermore, colonies are frequently infested with destructive parasitic mites or other insect pests. Some of the most damaging hive parasites were recently introduced to European honey bee (Apis mellifera) populations from the related Asian honey bee (Apis cerana) species.

Honey bee viruses: At present, 23 different viruses are known to infect honey bees. Notably, some of these viruses can cause asymptomatic infections, and depending virus levels and/or the presence of other stressors, infections may go undetected [6]. In fact, it is rare for a colony to be completely virus free, even if it appears healthy.

Viruses have many routes of transmission within and between colonies. Infections may be contracted through contaminated nectar and pollen stored within colonies. Viral particles can be transmitted through contact with infected individuals from the same hive, or when infected bees drift to a different hive. Male bees can infect virgin queens during mating (yes, bees have STDs too!) and infected queens may pass viruses to their offspring during egg-laying. Interestingly, many viruses found in honey bee colonies are not unique to honey bees and can be found in other invertebrate species (as summarized in [6]). Thus, interspecies transmission adds another dimension to viral dissemination amongst honey bee populations. For example, honey bees and bumble bees visiting the same flower may pass viral particles to one another through contaminated pollen [7]. Finally, Varroa mites (discussed in the next paragraph) are important vectors of honey bee viruses.

Honey bee viral infections are exacerbated by Varroa mites: Though some viruses alone are associated with colony decline and/or death, damage inflicted by other common viruses is greatly exacerbated by the presence of Varroa destructor mites [6]. Varroa mites are parasitic mites that feed on bee blood (much like ticks feed on vertebrate blood). Mites reproduce on pupating bees which has serious consequences for bee development. During pupation, larval bees (analogous to caterpillars) undergo metamorphosis to emerge as the familiar winged-adult bees (analogous to butterflies) we see visiting flowers. Unfortunately, while feeding on bee pupae, Varroa mites transmit viruses and immunosuppress their honey bee hosts [8], making them susceptible to newly contracted or pre-existing infections. Moreover, the feeding (and associated viral infections) exacts an energetic toll that can be detected weeks after bees emerge as adults [9]. This combination of nutritional stress and disease can shorter worker lifespan. In the most severe cases, viral infection aggravated by mite feeding during pupation results in the emergence of deformed adult bees and/or bees that exhibit paralytic (shaking/stumbling) symptoms. Such worker bees are short lived and do not contribute to colony productivity.

Varroa mites are an invasive parasite of European honey bee populations: Varroa mites are endemic to eastern Asia where they co-evolved with Asian honey bees (Apis cerana) (as summarized in [10]). However, during the mid-twentieth century Varroa mites gained access to European honey bee (Apis mellifera) populations when beekeepers brought both species of bees into intersecting geographic ranges. Varroa mites quickly gained a global distribution throughout A. mellifera populations and were first discovered in the US in 1987. As their name suggests, Varroa destructor mites are extremely destructive in European honey bees and mite presence is tightly correlated with colony losses throughout North America and Europe. Varroa mites are also cited as a major driver of the loss of feral honey bee populations in the US. The rapid spread and high virulence of Varroa mites in European honey bee populations is characteristic of invasive parasites. Frequently, parasites that successfully traverse host species boundaries are more damaging to their new host species since the new host has not evolved behavioral or physiological defense mechanisms. Indeed, Varroa destructor is not nearly as damaging to its original Asian honey bee host.

Nosema ceranae is an invasive fungal parasite of European honey bee populations: Interaction between honey bee species has also lead to the transmission of another parasite, Nosema ceranae, from Asian to European honey bees (as summarized in [11]). N. ceranae is a fungal pathogen that is transmitted via the fecal/oral route. Once eaten by a bee, N. ceranae spores germinate inside the bee's midgut (analgous to the stomach and small intestine) and invade midgut cells, where the parasite begins replicating. N. ceranae infection is energetically costly since reproductive parasitic states not only damage the lining of their host's digestive tract, but also commandeer energy molecules from their host. Infection increases host hunger levels and accelerates the pace at which workers progress through age-related tasks. Faster task progression ultimately shortens worker life span and threatens the careful balance of labor division within colonies. Heavily infected colonies are less productive and in some cases may succumb to N. ceranae infection.

Nosema ceranae is related to Nosema apis, another honey bee fungal parasite that coevolved with European honey bees (as summarized in [11]). N. apis has similar infection costs to N. ceranae, but infections are generally less damaging. N. ceranae's recent invasion of European honey bees from Asian honey bee population is of great concern. Like Varroa destructor, N. ceranae may be more virulent in European honey bees than in Asian honey bees since European honey bees have not had a chance to evolve defense mechanisms. N. ceranae is particularly damaging in A. mellifera iberiensis honey bee populations in Spain, where infection is strongly associated with colony death. In other parts of the world, however, N. ceranae does not inflict as much damage and it is thought that numerous factors, including temperature/climate, presence of other stressors (e.g. other diseases, pesticides, etc) and regional differences in host or parasite strain modulate N. ceranae virulence.

Honey bees host other fungal and bacterial pathogens: Aside from mite/viral interactions and Nosema infection, honey bee colonies may be plagued by other fungal and bacterial pathogens. Notably, the fungus Ascosphaera apis and the bacteria Paenibacillus larvae, attack larval honey bee stages. A. apis, the causative agent of chalkbrood, kills and mummifies bee larvae, producing fungal spores that can contaminate adult workers removing diseased larvae [12]. Adults can then pass the fungal spores to healthy larvae. Strong colonies usually are able to clear chalkbrood infestation, but weak colonies are susceptible. On the other hand, P. larvae, the cause of American foulbrood, devastates colonies unless control measures are taken [13]. Honey bee larvae are quickly killed by infection and the bacterium converts the host's remains into stringy brown goo that is full of durable bacteria spores. Spores persist for decades, and infections quickly sweep through apiaries, killing colonies. Infections are so highly contagious and damaging that disease eradication efforts require hives to be humanely killed and for contaminated equipment to be burned. (Alternatively, contaminated equipment can be sanitized by gamma ray exposure, but access to sterilization facilities is limited).

Small hive bees are an invasive pest of honey bees: Small hive beetles (SHB; Aethina tumida) are minor pests/opportunistic predators of African A. mellifera subspecies (reviewed in [14, 15]). Recently, SHBs were introduced to A. mellifera populations in Europe, North America (1996) and Australia. SHB adults invade colonies and lay eggs on colony food stores or larval/pupal honey bee stages. SHB eggs hatch and beetle larvae consume hive resources and/or immature bees. Furthermore, beetle larvae defecate in honey, resulting in fermentation and the spoiling of the colony's overwintering food supplies. Once ready to pupate, SHB larvae exit the colony and burrow into the soil until they emerge as adult beetles. Adults are strong fliers and can disperse to other colonies.

In their native range, SHB may actually be beneficial, because they prey on diseased, weak colonies (reviewed in [14, 15]). African bees also have behavioral defenses and will abscond, leaving infested hives behind. European A. mellifera populations, however, are far less likely to abscond and can become overrun by SHB. Climate currently constrains SHB range and virulence in the US. SHB are most problematic in warmer, moisture regions, where beetles may go through several generations per year.

Honey bees and chemical exposure

Honey bees are routinely exposed to natural and human applied chemicals (as reviewed in [16]). Pollen and nectar, the components of honey bee diet, contain diverse plant-produced chemicals. Honey bee digestive systems efficiently extract nutrients from nectar and pollen, while bee fat body tissue (analogous to human livers) can detoxify some plant-based food components that are harmful to bees [17]. However, beekeepers may enlist numerous chemicals to control hive parasites and pests. Meanwhile, agricultural systems are treated with pesticides, fungicides and herbicides. Exposure to beekeeper applied treatments or crop chemicals can have negative effects on honey bee health, productivity and survival as bee detoxification systems may not be able to fully or efficiently eliminate human applied chemicals.

Beekeeper applied chemicals: Ironically, many chemicals intended to control colony parasites or pests have been shown to have negative sublethal, effects on honey bee health. For example, coumaphos and fluvalinate are synthetic miticides used to kill Varroa mites. However, studies indicate that both chemicals can accumulate in honey bee colony wax and increase larval mortality. Likewise, naturally derived chemicals such as the essential oil thymol (also used as a miticide) can alter adult worker physiology and behavior.

Agricultural chemicals: Farmers apply pesticides, fungicides and herbicides to their crops to control insect pest populations, crop diseases and weeds. Some of these chemicals, especially pesticides, are highly toxic to honey bees and direct contact during spraying can result in sudden death. Such "pesticide-related bee kills" can be avoided if plants are not sprayed while in bloom (since bees will be attracted to flowers) or if plants are sprayed at night when honey bees are not active. However, bees may be exposed to lingering chemical residues while visiting flowers and return to their colonies with contaminated pollen and/or nectar. While exposure to smaller/diluted chemical doses may not directly kill bees, bees may suffer a host of sublethal effects including: learning deficits, impaired immune function, increased larval mortality and shortened adult life-span. These subtler costs weaken hives and increase their susceptibility to other stressors.

Neonicotinoids are a class of systemic pesticides: Neonicotinoids are a newer generation of pesticides that act as insect neurotoxins [16]. Approved for use in the 1990s, neonicotinoids represent approximately 30% of the global pesticide market and are valued at ~$3.6 billion USD (2011) [18]. Reasons behind the quick adoption and popularity of neonicotinoids are manifold. First neonicotinoids are less toxic to humans, other vertebrate animals and other beneficial insects than older generations of pesticides such as organophosphates. Second, neonicotinoids can systemically protect plants. Most neonicotinoids (~60%) are applied as seed or soil treatments. Growing plants absorb the pesticide and carry it throughout all their tissues, including roots, shoots, leaves, pollen and nectar. Ubiquitous pesticide presence in plant tissue protects the entire plant from herbivores whereas non-systemic pesticide treatments only protect areas of the plant that they are applied to. Third, as neonicotinoids are relatively new, pests that have developed resistance to other chemicals may still be susceptible to neonicotinoids, offering growers better control. Unfortunately, there is a large and growing body of evidence that some neonicotinoids can have detrimental sublethal effects on pollinators (as summarized in [18]). Because systemic neonicotinoids are found in plant nectar and pollen, pollinators may be exposed to small pesticide doses while foraging on treated crops. Furthermore, neonicotinoids applied to seeds are not completely absorbed by growing plants, resulting in contamination of soil and groundwater, again potentially exposing pollinators and other non-target insects to neurotoxins [19]. However, the majority of experiments investigating pollinator susceptibility to neonicotinoids have been conducted under laboratory or semi-field conditions using honey bees as a model organism. The only field study to date found no significant effect of proximity to fields with neonic coated seeds on honey bee colony health, though significant negative impacts on bumble bee colonies and solitary bee populations were recorded (as summarized in [18]). Additional field studies are desperately needed to validate these early findings. However, field studies are notoriously challenging and expensive; experiments must include many colonies and replicate field sites in order to have statistical power and have a reasonable time-line for observing effects.

Currently neonicotinoid use is contentious due to potential negative effects on pollinators in addition to concerns that neonicotinoids can translocate to and persist in soil and water, thereby invading ecosystems beyond farms and harming other non-target organisms.

Chemicals accumulate in colony wax: Due to their chemical structure, many chemicals applied to colonies or agricultural systems are absorbed by and are stable in fatty substrates, such as wax. In 2007-08, Penn State researchers tested wax and pollen (pollen contains fats) samples from hundreds of honey bee colonies for 200 chemical residues and found 121 different beekeeper or agricultural compounds, with each wax sample containing an average of 6 different residues [20]. Some of the most frequently found chemicals in pollen and/or wax samples were the miticides coumaphos and fluvalinate (applied by beekeepers to control Varroa infestation) and a fungicide, chlorothalonil. Each of these 3 commonly found chemicals has been shown to sublethal effects on larval bees and certain combinations result in synergistic toxicity [21]. The fact that an average of 6 different chemicals are found in wax samples is of concern since these chemicals may interact to with negative, synergistic toxicity consequences.

For further information, please see the "Bee Health" issue of Current Opinion in Insect Science. This issue contains 19 articles covering topics from genomics to ecology, reviewing our current state of knowledge on pollinator health, and providing creative and concrete ideas for the next steps in tackling these issues.

[3] Page Jr RE, Peng CYS: Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp Gerontol 2001, 36(4-6):695-711.

[4] Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D: Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 2006, 15(5):645-656.

[5] Cremer S, Armitage SAO, Schmid-Hempel P: Social immunity. Current Biology 2007, 17(16):R693-R702.

[6] McMenamin AJ, Genersch E: Honey bee colony losses and associated viruses. Current Opinion in Insect Science 2015, 8(0):121-129.

[7] Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, Vanengelsdorp D, Lipkin WI, Depamphilis CW, Toth AL, Cox-Foster DL: RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One 2010, 5(12):e14357.

[8] Yang X, Cox-Foster D: Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(21):7470-7475.

[9] Alaux C, Dantec C, Parrinello H, Le Conte Y: Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees. BMC Genomics 2011, 12(1):496.

[10] Rosenkranz P, Aumeier P, Ziegelmann B: Biology and control of Varroa destructor. Journal of Invertebrate Pathology 2010, 103, Supplement(0):S96-S119.

[11] Holt H, Grozinger C: Towards an integrated pest management (IPM) approach for Nosema parasites in honey bee (Apis mellifera) colonies. Unpublished manuscript 2015.

[12] Evison SEF: Chalkbrood: epidemiological perspectives from the host-parasite relationship. Current Opinion in Insect Science 2015, 10(0):65-70.

[13] Hansen H, Brødsgaard CJ: American foulbrood: a review of its biology, diagnosis and control. Bee World 1999, 80(1):5-23.

[14] Cuthbertson AG, Wakefield ME, Powell ME, Marris G, Anderson H, Budge GE, Mathers JJ, Blackburn LF, Brown MA: The small hive beetle Aethina tumida: A review of its biology and control measures. Current Zoology 2013, 59(5):644-653.

[15] Neumann P, Evans JD, Pettis JS, Pirk CW, Schäfer MO, Tanner G, Ellis JD: Standard methods for small hive beetle research. Journal of Apicultural Research 2013, 52(4):1-32.

[16] Johnson RM: Honey Bee Toxicology. Annual Review of Entomology 2015, 60(1):415-434.

[17] Berenbaum MR, Johnson RM: Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science 2015, 10(0):51-58.

[18] Godfray HCJ, Blacquière T, Field LM, Hails RS, Petrokofsky G, Potts SG, Raine NE, Vanbergen AJ, McLean AR: A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators, vol. 281; 2014.

[19] Krupke CH, Long EY: Intersections between neonicotinoid seed treatments and honey bees. Current Opinion in Insect Science 2015, 10(0):8-13.

[20] Mullin C, Frazier M, Frazier J, Ashcraft S, Simonds R, vanEngelsdorp D: High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health. PLoS One, 5(3):e9754.

[21] Zhu W, Schmehl DR, Mullin CA, Frazier JL: Four Common Pesticides, Their Mixtures and a Formulation Solvent in the Hive Environment Have High Oral Toxicity to Honey Bee Larvae. PLoS One 2014, 9(1):e77547.