Two species of microsporidia are known to infect honey bees, Nosema apis Zander (1909) and Nosema ceranae Fries (1996). Both species are obligate intracellular parasites, infecting the epithelial cells of the honey bee midgut (Larsson, 1986), however
N. ceranae has additionally been detected in the tissues of the hypopharyngeal glands,
salivary glands, malphigian tubules, and fat body (Chen et al., 2009). Once ingested, spores germinate in the lumen of the midgut of adult honey bees and rapidly produce more spores intracellularly (Bailey, 1955; Fries, 1988; Fries, 1989; Fries et al.,1992).
Nosema spp. spores are likely acquired by young house bees when they remove fecal
deposits, dead and diseased bees, and other foreign or contaminated material from the hive (Fries, 1997). Spores may also be ingested through contaminated food and at common water sources (Fries, 1997).
Spores of both species build up to extremely high levels in the lumen and within the midgut epithelial cells, and high levels of infection ultimately decrease the lifespans of infected bees (Fries, 1988; Fries et al., 1992; Higes et al., 2007a; Higes et al., 2007b; Paxton et al., 2007, Woyciechowski and Moron, 2009), Additionally, at the colony level, elevated Nosema sp. infection levels are correlated with higher supercedure rates and greater overwintering losses than those of uninfected colonies (Farrar, 1942).
Elevated infection levels may also severely interfere with nutrient absorption (Malone and Gatehouse, 1998) and ultrastructural alteration of cellular organelles (Wang and Moeller, 1971), leading to energetic stress and physiological and behavioral changes related to hunger, feeding, flight, and precocious foraging in honey bees (Mayack and Naug, 2009; Naug and Gibbs, 2009a; Kralj and Fuchs, 2010; Goblirsch et al., 2013). Foraging bees within a colony are known to contain the highest loads of Nosema sp. spores and, given their critical role in resource acquisition, this could affect the development and survival of colonies containing high levels of Nosema sp. spores (El- Shemy and Pickard, 1989; Smart and Sheppard, 2012).
Since 2007, N. ceranae has been found in populations of the western honey bee,
A. mellifera, throughout much of the world including the U.S., Canada, South and Central
America, Europe, North Africa, and Australia (Higes et al., 2006; Huang et al., 2007; Klee et al., 2007; Paxton et al., 2007; Calderon et al., 2008; Chen et al., 2008; Williams et al., 2008; Giersch et al., 2009; Higes et al., 2009). The current worldwide distribution of
N. ceranae appears to be the result of a host switch or range expansion, although when
this event occurred remains unclear (Chen et al., 2008; Klee et al., 2007; Paxton et al., 2007). However, evidence suggests that N. ceranae existed in U.S. managed honey bee populations as far back as the 1990s (Chen et al., 2008).
Cage studies have shown N. ceranae to be more virulent than N. apis (Higes et al., 2007a; Paxton et al., 2007) and Martin-Hernandez et al., (2007) found it to have a more sustained presence in the hive throughout the year, thus alarming beekeepers and scientists alike to the potential negative consequences of a new omnipresent
N. apis, leads to suppression of the humoral immune response (Antunez et al., 2009). The
relatively recent detection of N. ceranae in populations of A. mellifera implicated it as a potential contributing factor to Colony Collapse Disorder (CCD) (Higes et al., 2007a; Martin-Hernandez et al., 2007; Cox-Foster et al., 2007).
1.7.2 Varroa spp.
The genus Varroa (Acari: Varroidae) is composed of several specialized species of obligate ectoparasitic mites that feed on the hemolymph of bees from the genus Apis (Anderson and Trueman, 2000). Varroa jacobsoni Oudemans (1904), originally infesting the Asian honey bee, Apis cerana (Koeniger, et al., 1981), underwent a host shift
approximately around 1957, enabling it to parasitize the European honey bee, Apis
mellifera, present alongside Apis cerana colonies in Asia. This expanded host range,
coupled with the commercial movement of honey bee colonies, ultimately led to the nearly cosmopolitan distribution of V. jacobsoni (Anderson and Trueman, 2000). Further genetic analyses of V. jacobsoni demonstrated it to be a species complex composed of two sibling species: V. jacobsoni and Varroa destructor Anderson and Trueman (2000).
Varroa destructor is the most destructive pest of honey bee colonies worldwide,
reproducing in brood cells and parasitizing both immature and adult bees (Ritter et al., 1984; Martin, 1994; Martin, 1995; Martin, 1998; Oldroyd, 1999; Martin, 2001; Romero- Vera and Otero-Colina, 2002; Guzman-Novoa et al., 2010). Varroa destructor levels tend to build through the summer when the queen is laying up to 2,000 eggs per day and ample brood is present to parasitize. Mated adult female mites may produce 4-6
rapidly, killing or severely weakening bees going into winter (Amdam et al., 2004a). As a result, V. destructor mite infestation has been determined to be a primary, as well as interactive, cause of colony losses, and is particularly implicated in overwinter mortality (Dahle, 2010; Guzman-Novoa et al., 2010; LeConte et al., 2010).
Mites can affect the physiology of worker bees in infested colonies, causing weight loss, decreasing hemolymph carbohydrate and protein levels, including
vitellogenin titers, and suppressing the immune response, including both humoral and cellular immunity (Bowen-Walker and Gunn, 2001; Amdam et al., 2004a; Gregory et al., 2005; Yang and Cox-Foster, 2005). Honey bees with depleted levels of vitellogenin have fewer protein reserves to access during the pollen-limited overwintering period inside the colony and, therefore, could reduce longevity and/or increase susceptibility to pathogens and parasites over the winter due to their suppressed immune system.
Furthermore, V. destructor is known to be associated with the prevalence of certain honey bee viruses (Nordstrom, 2003, Chen et al., 2004, Tentcheva et al., 2004; Shen et al, 2005a; Shen et al., 2005b; Chen et al., 2006) both through the direct
transmission of viruses to brood and via the suppression of the honey bee immune system (Bowen-Walker et al., 1999; Yang and Cox-Foster, 2005). The presence of high V.
destructor infestation levels potentially allows viruses and other microbes to replicate
more readily in colonies highly infested with V. destructor (Yang and Cox-Foster, 2007).
Varroa destructor continues to be a main factor in honey bee colony losses,
despite the continued production and use of many miticides to control the pest. Monitoring and sampling of colonies for Varroa mites is a must for any serious and sustainable beekeeping operation in the 21st century. Further, selection and breeding for
genetic traits, such as “hygienic behavior” (HYG) or “Varroa-sensative hygiene” (VSH), provide beekeepers an additional, non-chemical, tool in their toolkit for combating
Varroa mites (Spivak and Gilliam, 1998; Spivak and Reuter, 2001; Ibrahim and Spivak,
2006). Bees that exhibit HYG traits are able to detect, uncap, and remove both Varroa- infested and diseased (P. larvae, A. apis) brood from the colony, while VSH bees exhibit more extreme hygienic behavior coupled with some degree of mite suppression, though the mechanism remains unknown. Selecting for such genetic traits that take advantage of the innate fastidiousness of certain bees lines to detect and remove infested pupae offer a more sustainable, long-term solution to the ongoing problem; one to which mites are unlikely to develop the resistance, or leave behind the harmful residues, associated with many commonly used, beekeeper-applied miticides.