The Synergistic Effects of Almond Protection Fungicides on Honey Bee (Hymenoptera: Apidae) Forager Survival

Abstract

The honey bee (Apis mellifera L.) contributes ∼$17 billion annually to the United States economy, primarily by pollinating major agricultural crops including almond, which is completely dependent on honey bee pollination for nut set. Almond growers face constant challenges to crop productivity owing to pests and pathogens, which are often controlled with a multitude of agrochemicals. For example, fungicides are often applied in combination with other products to control fungal pathogens during almond bloom. However, the effects of fungicides on honey bee health have been so far understudied. To assess the effects of some of the top fungicides used during the 2012 California almond bloom on honey bee forager mortality, we collected foragers from a local apiary and exposed them to fungicides (alone and in various combinations) at the label dose, or at doses ranging from 0.25 to 2 times the label dose rate. These fungicides were Iprodione 2SE Select, Pristine, and Quadris. We utilized a wind tunnel and atomizer set up with a wind speed of 2.9 m/s to simulate field-relevant exposure of honey bees to these agrochemicals during aerial application in almond fields. Groups of 40-50 foragers exposed to either untreated controls or fungicide-laden treatments were monitored daily over a 10-d period. Our results showed a significant decrease in forager survival resulting from exposure to simulated tank mixes of Iprodione 2SE Select, as well as synergistic detrimental effects of Iprodione 2SE Select in combination with Pristine and Quadris on forager survival.

The effects of iprodione fungicide on survival, behavior, and brood development of honeybees (Apis mellifera L.) after one foliar application during flowering on mustard

“…However, in recent years there have been some conflicting information from studies which have questioned the safety of this product to pollinators (Mussen et al (2004); Ladurner et al 2005Ladurner et al , 2008Fisher et al 2017). The product has been registered for several decades now and has played a critical role in significantly improving yields for farmers, especially in critical crops such as almonds in California and oil seed rape in Canada.…”

“…Especially with insecticides, eliminating the pest while protecting the pollinators can be a difficult task because most pollinators are insects that share a similar physiology. However, fungicide loads in pollen are often higher than any other pesticide category (Pettis et al 2013), and some studies have shown that fungicides can affect the pollinators if sprayed (Fisher et al 2017) or ingested (Mussen et al 2004) at certain doses. Even though a fungicide is targeted at very different organisms, the physiology of fungal pathogens (e.g., Sclerotinia sclerotiorum, which causes sclerotinia stem rot) is considerably different from that of the honeybee.…”

“…Recently, there have been some open literature studies that have linked effects on honeybee larvae and foragers to the use of iprodione (Mussen et al 2004;Ladurner et al 2005Ladurner et al , 2008Fisher et al 2017). It is effective against spores and mycelium of a number of parasitic fungi.…”

“…Thus, the mode of action of a fungicide should theoretically pose a lesser hazard to pollinators. However, fungicide loads in pollen are often higher than any other pesticide category (Pettis et al 2013), and some studies have shown that fungicides can affect the pollinators if sprayed (Fisher et al 2017) or ingested (Mussen et al 2004) at certain doses. There are synergistic effects reported for fungicides used in combination with insecticides (Colin and Belzunces 1992;Pilling and Jepson 1993;Thompson and Wilkins 2003), for example, if fungicides inhibiting ergosterol biosynthesis are combined with pyrethroids or cyano-substituted neonicotinoids.…”

“…Rovral, a formulated product of iprodione, is widely used to control various fungal pathogens in crops such as almonds in California and oil seed rape in Canada. Recently, there have been some open literature studies that have linked effects on honeybee larvae and foragers to the use of iprodione (Mussen et al 2004;Ladurner et al 2005Ladurner et al , 2008Fisher et al 2017). However, these studies discuss either only the intrinsic toxicity of the compound based on laboratory studies or studies conducted at use rates much higher than actual field applications.…”