Ecological and evolutionary approaches to managing honeybee disease

Abstract

Honeybee declines are a serious threat to global agricultural security and productivity. Although multiple factors contribute to these declines, parasites are a key driver. Disease problems in honeybees have intensified in recent years, despite increasing attention to addressing them. Here we argue that we must focus on the principles of disease ecology and evolution to understand disease dynamics, assess the severity of disease threats, and control these threats via honeybee management. We cover the ecological context of honeybee disease, including both host and parasite factors driving current transmission dynamics, and then discuss evolutionary dynamics including how beekeeping management practices may drive selection for more virulent parasites. We then outline how ecological and evolutionary principles can guide disease mitigation in honeybees, including several practical management suggestions for addressing short- and long-term disease dynamics and consequences.

Fig. 1. Honeybee colony losses.

a, A typical managed honeybee colony. b, Colony numbers (in millions) in the United States between 1943 and 2016. c, United States winter colony losses between 2006 and 2015^,. d, Breeding season colony losses in England and Wales between 2002 and 2010. Data in c,d were obtained from graphs in their respective source papers^, using WebPlotDigitizer (http://arohatgi.info/WebPlotDigitizer/app/). Photo credit: K.S.D.

Fig. 2. Parasites threatening honeybees.

a, Varroa destructor mite (indicated with arrow) attached to a foraging worker bee. b, Spores of the microsporidian Nosema ceranae in a honeybee ventricular cell. c, Small hive beetle (Aethina tumida) larvae infesting a honeybee colony frame. d, A honeybee with deformed wings, caused by infection with deformed wing virus; the arrows point at Varroa mites, which vector and amplify the virus. e, A disintegrating honeybee pupa as a result of infection with the American foulbrood bacterium Paenibacillus larvae. f, Honeybee pupa infected with the fungus Ascosphaera apis, which causes chalkbrood disease. g, Tracheal mites (Acarapis woodi) infesting honeybee tracheae. h, A parasitoid fly (Apocephalus borealis) larva (arrow) bursting out of an infected honeybee. Photo credits: Jennifer Berry (a); Mariano Higes (b); Jamie Ellis (c); Paul Kruse at KnackbockBlog (d); Western Australian Agriculture Authority (Department of Agriculture and Food, WA (e); Ron Snyder at the Bee Informed Partnership (f); USDA (g); John Hafernik (h).

Fig. 3. Beekeeping results in high bee densities and movement.

a, Wild and feral honeybees, that is, those that have escaped management and are living outside of the realm of direct human influence, live in single colonies that are typically hyperdispersed in the landscape. b, At the other extreme, intensively managed bees are kept in hyperconcentrated bee yards with hundreds or even thousands of colonies. c,d, Most of these operations are migratory, moving their colonies several thousand miles around states, countries and continents to provide pollination services for seasonal crops. It is estimated that between one-half and two-thirds of all managed colonies in the US are moved to the almond orchards of California’s Central Valley in late February and early March. Thus, transmission potential among these bees can be thought of as nearly global, since long-range movement is combined with high potential for contacting other bee colonies. Photo credits: Vitaliy Parts/Alamy Stock Photo (a); Dariya Angelova/Alamy Stock Photo (b); ZUMA Press, Inc./Alamy Stock Photo (c).

The importance of hive density on infectious disease spread.

a, A simple disease dynamics model can be applied to honeybee parasites, in which colonies are either susceptible (S) or infected (I) with the parasite. Colonies die at a background rate d and become infected at the rate βSI, in which β is the transmission parameter. Infected colonies experience an additional mortality rate, α, due to parasite infection. In this model, no new colonies are added, thus representing a situation in which disease dynamics are studied in apiaries with a fixed starting density of colonies. b, Graphical representation of colonies maintained at low density (left) and high density (right). c, Disease dynamics over 20 bee generations based on the model shown in panel a, and with low density (20 colonies per apiary) or high density (200 colonies per apiary). Densities of susceptible (S), infected (I) and total (N) colonies are shown. At higher densities, parasites spread much more rapidly and cause greater proportional colony losses. (Parameter values used: I(0) = 1, d = 0.01, β = 0.15, α = 0.1.)

Fig. 4. Management applications.

a, Transmission reduction is a key management goal to reduce both ecological disease pressure and selection for greater parasite virulence; transmission reduction should occur at multiple scales, including the two shown here: between colonies within an apiary, and at continental scales. b, Promoting ‘survivor stock’, that is, allowing colonies with low parasite resistance to naturally die can increase the evolution of honeybee resistance. c, Increased colony-level genotypic diversity improves disease outcomes and supports general colony health, and may also reduce selection pressure for increased virulence evolution. d, Increased dietary diversity and reduced dependence on processed sugars can support better bee health and disease resistance, both for individual bees and for group-level defences.