**5. Adjuvants**

*Modern Beekeeping - Bases for Sustainable Production*

**3.1 Chitin synthesis inhibitors**

**3.2 Juvenile hormone mimics**

affects survival of honey bee foragers [69].

**3.3 Ecdysone receptor antagonists/agonists**

with the three categories, and commonly used in agricultural and horticultural cropping systems, directly or indirectly negatively affect honey bees [6].

toxic to honey bees and negatively affects brood production [64].

Chitin synthesis inhibitors disrupt molting of insect larvae by interfering with enzymes responsible for stimulating the synthesis and formation of chitin, an important component of the insect exoskeleton [27, 53, 56, 59, 60]. Studies demonstrate that the chitin synthesis inhibitor, diflubenzuron, negatively affects learning behavior [56], decreases the number of adult honey bees [58], and reduces larval and queen survival [9, 57, 58]. Consequently, this impacts brood production in whole colonies [57, 61–63]. Another chitin synthesis inhibitor, novaluron, is directly

Juvenile hormone mimics (analogs) arrest development and cause insects to remain in an immature stage, which inhibits adult emergence and prevents insects from completing their life cycle [27, 53, 60, 65]. The juvenile hormone mimic, fenoxycarb, affects adult worker honey bees [66], causes adults to age prematurely [67], and, in whole colonies, causes extensive mortality of honey bee larvae, thus reducing the number of brood and size of over-wintering colonies in the subsequent year [58]. In addition, exposure to fenoxycarb affects the ability of colonies to overwinter, which reduces winter survival [58]. The juvenile hormone mimic, pyriproxyfen, affects synthesis and accumulation of vitellogenin (protein in hemolymph from which egg yolk is derived) in young worker bees [68] and negatively

Ecdysone receptor antagonists/agonists are insect growth regulators that disrupt molting by inhibiting metabolism of the molting hormone, ecdysone, or they bind to ecdysone receptors, resulting in premature molting of larvae or nymphs, and eventually death [54, 60, 70, 71]. Methoxyfenozide does not exhibit any harmful effects on honey bee larvae or adults [9] although Fisher et al. [69] reported that methoxyfenozide negatively affected the survival of honey bee foragers. In general, tebufenozide has been shown to exhibit no direct or indirect harmful effects to honey bee colonies or queen development [58]; however, Abramson et al. [56] found that tebufenozide negatively affected the learning behavior of honey bee adults. Azadirachtin does not indirectly effect brood production, with only minimal harmful effects to honey bee colonies by negatively affecting overwintering sur-

Herbicides are the most widely used pesticides in agricultural and horticultural cropping systems for control of unwanted vegetation or plant material [27, 35, 72]. Therefore, herbicides should have minimal, if any, direct or indirect effects on honey bees [34, 73, 74]. The post-emergent herbicides, dicamba and picloram, were found not to be directly harmful to adult honey bees or brood [73, 74]. However, the contact, post-emergent herbicide, paraquat, was reported to be directly harmful to honey bees [75]. In addition, laboratory studies found that honey bee colonies

**4**

vival [58].

**4. Herbicides**

Honey bees are exposed to a multitude of pesticides while foraging for pollen and nectar in flowering plants, and many formulated pesticides that are applied to control insect and mite pests, or diseases typically contain adjuvants [5, 7, 8]. Therefore, honey bees are likely being directly exposed to adjuvants when foraging [7]. Adjuvants are compounds that are a component of the pesticide formulation (as an "inert ingredient") or are added as a tank-mix additive [86, 87]. Adjuvants are designed to enhance the effectiveness of pesticides, including insecticides and herbicides, by improving or altering deposition, increasing toxicity, improving mixing ability, and/or extending residual activity or persistence [86].

Some of the most widely used adjuvants are surfactants that increase pesticide efficacy by reducing the surface tension of spray droplets, which allows the spray solution to cover more leaf surface area—especially waxy or hairy leaf surfaces of certain plants [5, 7, 88]. In addition, surfactants have been shown to have insecticidal and miticidal properties [89–92]. Initially, surfactants were assumed to be biologically inert with no direct or indirect harmful effects to honey bees [7, 93]. However, studies show that certain surfactants may be toxic to honey bees [88, 94, 95], especially the organosilicone surfactants, which are reported to exhibit direct and indirect harmful effects to honey bees [5, 7, 94, 96]. Nonetheless, the mechanism by which organosilicone surfactants indirectly affect honey bees, such as, impairing learning ability, is not known [5].

## **6. Conclusion**

The European or western honey bee, *Apis mellifera*, is exposed to a diverse array of pesticides when foraging on flowering plants for pollen and nectar. Although insecticides are commonly encountered, honey bees are also exposed to other pesticides (fungicides, insect growth regulators, and herbicides) and compounds (adjuvants) that can result in direct or indirect effects on individual honey bees,

thus affecting colony health. Therefore, it is important to understand the direct and indirect harmful effects of fungicides, insect growth regulators, herbicides, and adjuvants on honey bees, and implement measures that will reduce exposure of honey bees to these pesticides and compounds. These measures include: timing pesticide applications when honey bees are not present, avoid applying pesticides to flowering plants that are attractive to honey bees, select and apply pesticides that are less directly and indirectly harmful to honey bees, and follow specific requirements on pesticide labels regarding honey bee protection.
