Learning of a mimic odor combined with nectar nonsugar compounds enhances honeybee pollination of a commercial crop

Abstract

The increasing demand on pollination services leads food industry to consider new strategies for management of pollinators to improve their efficiency in agroecosystems. Recently, it was demonstrated that feeding beehives food scented with an odorant mixture mimicking the floral scent of a crop (sunflower mimic, SM) enhanced foraging activity and improved recruitment to the target inflorescences, which led to higher density of bees on the crop and significantly increased yields. Besides, the oral administration of nonsugar compounds (NSC) naturally found in nectars (caffeine and arginine) improved short and long-term olfactory memory retention in conditioned bees under laboratory conditions. To test the effect of offering of SM-scented food supplemented with NSC on honeybees pollinating sunflower for hybrid seed production, in a commercial plantation we fed colonies SM-scented food (control), and SM-scented food supplemented with either caffeine, arginine, or a mixture of both, in field realistic concentrations. Their foraging activity was assessed at the hive and on the crop up to 90 h after treatment, and sunflower yield was estimated prior to harvest. Our field results show that SM + Mix-treated colonies exhibited the highest incoming rates and densities on the crop. Additionally, overall seed mass was significantly higher by 20% on inflorescences close to these colonies than control colonies. Such results suggest that combined NSC potentiate olfactory learning of a mimic floral odor inside the hive, promoting faster colony-level foraging responses and increasing crop production.

Discovery of octopamine and tyramine in nectar and their effects on bumblebee behavior

“…Likewise, the interplay between the nectar constituents found here shows that phytochemical context can determine the pattern of downstream effects on bees. For humans, CA has behavioral effects that vary with phytochemical context ( Schuster and Mitchell, 2019 ), but this has not been considered through an ecological lens: like most nectar secondary metabolites, CA ’s effects on insects have historically been studied in isolation ( Baracchi et al., 2017 ; Thomson et al., 2015 ; Wright et al., 2013 , but see Estravis-Barcala et al., 2021 ; Marchi et al., 2021 ). Methylxanthines such as CA can synergize with OA ( Nathanson, 1984 ), potentially giving rise to the antagonistic effects observed here.…”

“…Despite nectar’s chemical diversity ( Palmer-Young et al., 2018 , 2019 ), our understanding of its effects on pollinators is limited in two key ways. First, though foliar chemical ecology highlights the relevance of synergistic effects ( Richards et al., 2016 ), research on the behavioral effects of nectar chemistry typically involves a small number of phytochemicals studied in isolation ( Adler, 2000 ; Stevenson et al., 2017 ), but see Estravis-Barcala et al., 2021 ; Hernández et al., 2018 ; Marchi et al., 2021 ; Richman et al., 2022 ; Thorburn et al., 2015 ). Secondly, though insect hormones and endocrine disruptors have long been identified in leaf tissues ( Bowers, 1991 ), whether nectar is a site of any analogous chemical “cross-talk” between plants and pollinators (as explored for floral volatiles by Schiestl, 2010 ) is an obvious question ( Mustard, 2020 ; Schultz and Appel, 2004 ).…”

Targeted crop pollination by training honey bees: advances and perspectives

“…Sugar syrup can be offered by means of in-hive feeders of different types, such as division board or top hive feeders. Such supplemental feeding practice is suitable for olfactory conditioning of colonies providing pollination services (Farina et al, 2020;Estravis-Barcala et al, 2021;Farina et al, 2022;Farina et al, 2023). Scented food can be obtained by diluting a small volume of the mimic odor (50 µL) per liter of sucrose solution (50% weight/ weight, henceforth: w/w).…”

“…When successful foragers return to the hive and display dances, the activation or reactivation of unemployed foragers is promoted, as well as, in a minor proportion, of those nestmates ready to initiate foraging tasks (Lindauer, 1954;Seeley, 1986;Seeley, 1995;Thom et al, 2007). Incoming foragers at the entrance of the hive can be counted for a short period (1 min) at the same time on consecutive days (Delaplane et al, 2013a;Farina et al, 2020;Estravis-Barcala et al, 2021;Farina et al, 2022;Farina et al, 2023;see Figures 4A, 5A as examples). Ideally, 3 to 5 independent measurements should be done before feeding the colonies to control for environmental conditions, pre-existing colony differences and behavioral inertia (Rodet and Henry, 2014).…”

Toward evidence-based decision support systems to optimize pollination and yields in highbush blueberry

“…A promising new approach to enhance recruitment is feeding honey bee and bumble bee colonies with caffeineor arginine-treated syrup flavored with crop flower scents just before bloom onset (Farina et al, 2020;Arnold et al, 2021;Estravis-Barcala et al, 2021a), training them to cropspecific rewards. Blueberry flower scents have been identified (Rodriguez-Saona et al, 2011;Forney et al, 2012;Huber, 2016) and could be used to aid bee recruitment.…”