Floral Sonication is an Innate Behaviour in Bumblebees that can be Fine-Tuned with Experience in Manipulating Flowers
J Insect Behav
Floral Sonication is an Innate Behaviour in Bumblebees that can be Fine-Tuned with Experience in Manipulating Flowers
Tan Morgan 0 1
Penelope Whitehorn 0 1
Gillian C. Lye 0 1
Mario Vallejo-Marín 0 1
0 Natural Power Consultants , Ochil House, Springkerse Business Park, Stirling, Scotland FK7 7XE , UK
1 Biological and Environmental Sciences, University of Stirling , Scotland FK9 4LA , UK
Bumblebees demonstrate an extensive capacity for learning complex motor skills to maximise exploitation of floral rewards. This ability is well studied in nectar collection but its role in pollen foraging is less well understood. Floral sonication is used by bees to extract pollen from some plant species with anthers which must be vibrated (buzzed) to release pollen. Pollen removal is determined by sonication characteristics including frequency and amplitude, and thus the ability to optimise sonication should allow bees to maximise the pollen collection. We investigated the ability of the buff-tailed bumblebee (Bombus terrestris) to modify the frequency and amplitude of their buzzes with increasing experience manipulating flowers of the buzz-pollinated plant Solanum rostratum. We analysed flight and feeding vibrations generated by naïve workers across feeding bouts. Feeding buzzes were of a higher frequency and a lower amplitude than flight buzzes. Both flight and feeding buzzes had reduced amplitudes with increasing number of foraging trips. However, the frequency of their feeding buzzes was reduced significantly more than their flight buzzes as bumblebee workers gained experience manipulating flowers. These results suggest that bumblebees are able to modify the characteristics of their buzzes with experience manipulating buzz-pollinated flowers. We discuss our findings in the context of bumblebee learning, and the current understanding of the optimal sonication characteristics for releasing pollen in buzz-pollinated species. Our results present a tantalising insight into the potential role of learning in floral sonication, paving the way for future research in this area.
Introduction
Bumblebees (Bombus spp.) play an important role in providing pollinator services in
both natural and agricultural systems
(Goulson 2003; Goulson et al. 2008)
. The genus
Bombus (Apidae) comprises approximately 250 species of medium-sized to large bees,
distributed around the world (Michener 2007). These species rely on pollen and nectar
as food sources, collecting these floral rewards from a diverse range of plant species
(Sladen 1912; Goulson 2010)
. Previous studies have shown that bumblebees are able to
learn to manipulate flowers with different morphologies
(Heinrich 1979; Laverty 1980;
Laverty and Plowright 1988; Laverty 1994; Raine and Chittka 2007, 2008)
and across
different contexts (Biernaskie et al. 2009), and that they can even learn from other
individuals of the same
(Leadbeater and Chittka 2008)
or different species (Goulson
et al. 2013). The ability to adjust their behavioural repertoire to manipulate flowers and
collect resources from diverse plant species allows bumblebees to maximise the
exploitation of floral resources over time, across different environments, and in distinct
plant communities.
Bumblebees can learn in order to exploit floral resources more proficiently, and at a
faster rate, with increasing experience in handling flowers
(Heinrich 1979; Laverty
1980; Laverty and Plowright 1988; Laverty 1994; Raine and Chittka 2007, 2008)
.
Previous work has shown that the amount of experience required to achieve maximum
proficiency increases with increasing floral complexity
(Laverty 1980, 1994)
. To date,
most research on bumblebee learning has focused on behaviours displayed with
relatively simple natural and artificial flowers in which nectar is used as the main
reward
(but see Raine and Chittka 2007; Kitaoka and Nieh 2009; Konzmann and
Lunau 2014; Lunau et al. 2015; Muth et al. 2016)
. In contrast, less is known about
whether and how bumblebees learn to manipulate complex flowers in which pollen is
the main or only reward. The optimal method for pollen removal varies among plant
species as a result of differing floral structure, anther morphology, and pollen properties
(Buchmann 1983; Thorp 2000)
.
In most flowering plants, anthers split lengthwise to passively release pollen, which
is then available for collection by pollinators
(Buchmann 1983)
. However, in a sizeable
number (around 20,000 species across a diverse suite of plant taxa), pollen is concealed
within poricidal anthers
(Buchmann 1983)
. These non-dehiscent, conical or tubular
anthers have an apical pore through which pollen is expelled only when the anthers are
vibrated
(Buchmann 1983; Harder and Barclay 1994; De Luca and Vallejo-Marín
2013)
. Some floral visitors, including Bombus, can release pollen from these structures
using a process known as sonication
(Buchmann 1983)
. During sonication, the bee
wraps its bod (...truncated)