Figure 1.2 Grooming, or mite‐chewing, is a heritable trait in which honey bees remove and kill adult Varroa mites by chewing off parts of the mite's body, carapace, or legs.
Figure 1.3 Hygienic behavior or Varroa Sensitive Hygiene (VSH), is a form of social immunity in which honey bees selectively remove the varroa‐infested larvae and pupae from beneath capped cells. The mites infecting these brood cells are killed along with the developing bee upon opening of the cell.
There exist multiple mechanisms of natural Varroa resistance, a form of behavioral social immunity, that have a genetic basis. These include grooming behavior, also known as “mite chewing,” and hygienic behavior, also known as Varroa Sensitive Hygiene (VSH). Grooming behavior is the process whereby worker bees kill mites by deftly chewing off the carapace, ventral plate, or legs of a mite (Figure 1.2). The strength of a colony's ability to groom Varroa mites is indicated by the percentage of chewed mites among the mites that fall onto a sticky board placed beneath a screened bottom board in a hive (Rosenkranz et al. 1997). Hygienic behavior is the process whereby worker bees remove diseased (or dead) brood from the cells in which they are (or were) developing (Figure 1.3). VSH is measured by determining the percentage of sealed brood cells that contain Varroa mites shortly after cell capping and then again shortly before brood emergence (cell uncapping). Because this assay of a colony's VSH behavior is rather tricky to perform, people often use a different assessment of hygienic behavior: the freeze‐killed brood (FKB) assay. Because the FKB assay does not involve Varroa infested brood, it is not a direct measure of VSH. The FKB assay works by freezing a c. 3 in. diameter circle of sealed brood cells, thereby killing the brood within, followed by calculating the percentage of the dead brood that have been removed, either 24 or 48 hours after the freezing of the brood (Spivak and Downey 1998).
In a long‐term study in Norway, variation among colonies in their resistance to Varroa was found to be based on neither grooming behavior nor hygienic behavior, but on something else that was hindering mite reproduction. Oddie and colleagues (2017) examined managed honey bee colonies that had survived in the absence of Varroa control for >17 years alongside managed colonies that had received miticide treatments twice each year. Records were kept of daily mite drop counts, and of assays of the colonies' mite grooming and hygienic behaviors, for both survivor and control colonies. No difference was found in the proportion of damaged mites (~40% chewed in colonies of both groups) or in FKB removal rates (only ~5% brood removed). However, the average daily mite‐drop counts (indicators of the mite populations in colonies) were 30% lower in surviving colonies compared to susceptible ones. Evidently, there were other colony factors (besides mite grooming and hygienic behaviors) responsible for reducing the reproductive success of the mites in these colonies of Norwegian honey bees. Since donor brood was used for the testing in both groups of colonies (mite susceptible and mite resistant), the possibility of protective traits of immature bees was eliminated. What Oddie et al. found is that in the mite‐resistant colonies (but not in the mite‐susceptible ones) the worker bees are uncapping brood cells and then recapping them several hours later, and that this reduces the mites' reproductive success to a level that protects the colony. An 80% reduction in mite reproductive success, together with a reduction in brood size, independent of grooming or hygienic behavior, was also described for populations of survivor (untreated) colonies of honey bees living on the island of Gotland in Sweden (Fries and Bommarco 2007; Locke and Fries 2011).
Good Lifestyle
To understand the survival of honey bee colonies living in the wild, we must look not only at their genetic makeup but also at their lifestyle. How do the ways in which wild colonies live combine with their genes to limit mite reproductive success and the virulence of mite‐vectored pathogens? We know that modern beekeeping practices create living conditions for managed colonies that are far more stressful than the living conditions of colonies living in the wild (see Table 1.1). For example, we know that the artificial crowding of colonies in an apiary, the provision of large hives which foster Varroa reproduction, and the suppression of swarming behavior – are all apicultural manipulations that make large honey harvests possible for the beekeeper but are harmful to colony health (Seeley and Smith 2015; Loftus et al. 2016). Another important, but little understood, stressor experienced by managed colonies is the greater thermoregulation stresses experienced by colonies living in a standard hive compared to in a bee tree (Mitchell 2016). Our modern beekeeping practices – launched in 1852 with the invention of the movable frame hive, by Lorenzo L. Langstroth – have created new challenges for honey bee colonies, which are adapted for living without human management (interference). For the remainder of this chapter, we will explore the lifestyle features that help wild colonies of honey bees thrive despite their pests, parasites, and pathogens. We will also draw lessons that beekeepers and bee doctors can employ to help promote the health of the managed colonies living in apiaries.
Part 1: The Environment of a Wild Colony
Cavity Size
A good place to begin our exploration of wild honey bee health is understanding the home of a honey bee colony found in nature (Figure 1.4). Wild honey bees predominately make their homes inside the cavities of hollow trees, though any cavity of appropriate volume and specific characteristics will do, and this includes manmade structures, rock crevices, and other spaces. Wild colonies choose small cavities, with an average volume of just 45 l (range 30–60 l: Seeley and Morse 1976; Seeley 1977). When honey bee colonies choose their nesting sites, they seek cavities of this size, which is substantially smaller than the typical Langstroth hive in an apiary, with a volume of 120–160 l (Root and Root 1908; Loftus et al. 2016).
Nest cavity size has a major impact on honey bee health through its effect on mite population dynamics. A brief review of the Varroa life cycle will help us understand the role of nest cavity size on a colony's mite population. Varroa mites have two different life phases: the phoretic phase in which adult mites feed on the “fat bodies” of honey bees and the reproductive phase in which mites reproduce in the cells of sealed brood of workers and drones (Rosenkranz et al. 2010). Only adult female mites are phoretic; both the tiny males and the nymphal stage females remain within the capped brood cells. Honey bee larvae are essential for the mite because it has no free‐living stage off the host – the mite is entirely dependent on honey bee brood for its own propagation. Honey bee colonies living in large hives hold more brood than those living in natural nest cavities, so colonies in large hives are especially favorable for mite reproduction.
Table 1.1 Characteristics of wild honey bees (Apis mellifera) that differ from managed honey bees and their impact on bee health.
| Characteristic | Wild colonies | Reference | Managed colonies | Reference |
|---|---|---|---|---|
| Colony lifespan |
Long‐lived 5–6 yr once established
|