Odor-Pollution From Fungicides Disrupts Learning and Recognition of a Common Floral Scent in Bumblebees (Bombus impatiens)

Abstract

Background and AimsBumblebees provide vital pollination services to both natural and agricultural ecosystems. Consequently their declines in species-diversity and population size over the last five decades is alarming. Direct contributors to these declines include pesticides, habitat loss, and disease. However, given that colony fitness is linked to foraging success, successful conservation requires mitigation of any anthropogenic practices that negatively impact foraging. Previous work has shown that agrochemical odor-pollution, including that of fungicides, can modulate bumblebee foraging behavior. This study investigates how odor pollution from three common fungicides (Safer® Brand Garden Fungicide II, Scotts® Lawn Fungus Control, and Reliant® Systemic Fungicide) affects Bombus impatiens’ floral-odor learning and recognition using an associative learning paradigm.MethodsThe effects of fungicide-odor pollution were tested in three ways: (1) background pollution during floral-odor learning; (2) background pollution during floral-odor recognition; and (3) point (localized) pollution during floral-odor recognition. Electroantennogram (EAG) recordings from B. impatiens confirmed the salience of all odor-stimuli and examined impacts of background fungicide-odor on antennal responses to floral-odor. To better understand how fungicide-odor structure related to behavioral data, scents were sampled (Solid Phase Microextraction) and analyzed using gas chromatography–mass spectrometry. Odors were then characterized using the Compounds Without Borders (CWB) vectorization method.ConclusionAll fungicides tested disrupted floral-odor learning and recognition for at least one concentration tested, and Scotts® was universally disruptive at all tested concentrations. All fungicides induced EAG responses, indicating they provide perceivable odor stimuli. Interestingly, two of three tested fungicides (Scotts® and Reliant®) inhibit antennal responses to Monarda fistulosa odor. Odor characterization supports previous findings that sulfurous scents could be disruptive to odor-driven foraging behaviors. Inability for foraging bumblebees to associate to rewarding floral odors in the presence of fungicidal odor pollution could have negative large-scale implications for colony health and reproductive fitness.

Behavioral state influences encoding mechanisms of color and odor integration in a model insect, the bumblebee Bombus impatiens

“…A subsequent study found variable effects of diesel-driven odor pollution dependent on floral color [14]. Interestingly diesel exhaust contains sulfurous components - an attribute shared by several fungicides that have also been shown to disrupt bumblebee behavior on a local scale [11,12].…”

“…In addition, anthropogenic activity can indirectly impact sensory signals that are utilized by bumblebees while foraging for floral resources. For example, negative effects of human activity on floral-scent signaling and reception include a reduction of distance traveled by floral scent [6,7], increased foraging times [8], decreases in floral scent recognition [9][10][11][12], and alterations of flower visitation rates [13,14]. These negative effects are potentially exacerbated by asymmetric impacts of sublethal pesticide exposure with odor-learning,but not color-learning, being impaired [15].…”

Fungicides and strawberry pollination–Effects on floral scent, pollen attributes and bumblebee behavior

“…Another potential explanation for the lower visit frequency could be the direct effect of fungicides on altering the taste, as shown with sugar water [ 70 ], which in turn can influence the foraging behaviour of bees. Furthermore, the scent of the used fungicides could have interfered with the recognition of common floral scent [ 71 ].…”

“…In this study, actual strawberry plants were used and last sprayed a few days before the trials leading to more random, but also natural variation in terms of olfactory and visual traits, compared to artificial flowers or scent feeders, as used in several other studies on strawberry pollination (e.g., [ 15 , 71 ]. Another critical aspect of fungicide use in crop cultivation that needs to be considered is that the fungicide treatment of the plants may affect not only the foraging behaviour of bumblebees but also the physiology of the insects.…”

A neonicotinoid pesticide alters Drosophila olfactory processing

“…Although these chemicals control pests and plant pathogens, non-target insects such as bees and butterflies encounter them while foraging from chemical-laden plants. These chemicals can also have non-consumptive effects, such as creating odor pollution, which makes olfactory-based tasks such as foraging and navigation challenging for insects 8 , 9 . However, once consumed, they have detrimental impacts on non-target insect health, which can persist for generations after exposure 10 – 14 .…”