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Bee and Floral Traits Affect the Characteristics of The bioRxiv preprint doi: https://doi.org/10.1101/494690; this version posted December 13, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Bee and floral traits affect the 2 characteristics of the vibrations 3 experienced by flowers during 4 buzz-pollination 5 6 Blanca Arroyo-Correa1,2 7 Ceit Beattie1 8 Mario Vallejo-Marín1,* 9 10 1 Biological and Environmental Sciences, School of Natural Sciences, University of Stirling. 11 Stirling, Scotland. FK9 4LA. Email: [email protected] 12 2 Integrative Ecology Group, Estación Biológica de Doñana (EBD-CSIC), Sevilla, Spain. 13 14 * Author for correspondence. Telephone: +44 (0) 1786 467822. Email: [email protected] 15 16 17 18 Running title: Bee and plant type affect floral vibrations 19 20 Key words: Buzz pollination, Bombus, substrate-borne vibrations, Solanum, sonication. 1 bioRxiv preprint doi: https://doi.org/10.1101/494690; this version posted December 13, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 21 Summary statement 22 We show that buzz-pollinating bumblebees differ in the type of vibrations produced while 23 visiting the same flower, and that floral species affects the transmission properties of those 24 vibrations. 2 bioRxiv preprint doi: https://doi.org/10.1101/494690; this version posted December 13, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 Abstract 26 During buzz pollination, bees use their indirect flight muscles to produce vibrations that are 27 transmitted to the flowers and result in pollen release. Although buzz pollination has been 28 known for >100 years, we are still in the early stages of understanding how bee and floral 29 characteristics affect the production and transmission of floral vibrations. Here we analysed 30 floral vibrations produced by four closely related bumblebee taxa (Bombus spp.) on two buzz- 31 pollinated plants species (Solanum spp.). We measured floral vibrations transmitted to the 32 flower to establish the extent to which the mechanical properties of floral vibrations depend 33 on bee and plant characteristics. By comparing four bee taxa visiting the same plant species, 34 we found that peak acceleration (PA), root mean-squared acceleration (RMS) and frequency 35 varies between bee taxa, but that neither bee size (intertegular distance) or flower biomass 36 (dry weight) affect PA, RMS or frequency. A comparison of floral vibrations of two bee taxa 37 visiting flowers of two plant species, showed that, while bee species affects PA, RMS and 38 frequency, plant species affects acceleration (PA and RMS) but not frequency. When 39 accounting for differences in the transmission of vibrations across the two types of flowers, 40 using a species-specific “coupling factor”, we found that RMS acceleration and peak 41 displacement does not differ between plant species. This suggests that bees produce the same 42 initial acceleration in different plants but that transmission of these vibrations through the 43 flower is affected by floral characteristics. 3 bioRxiv preprint doi: https://doi.org/10.1101/494690; this version posted December 13, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 44 Introduction 45 Buzz pollination is a fascinating interaction between flowers with specialised morphologies and 46 bees that use vibrations to remove pollen (Buchmann, 1983; Vallejo-Marin, in review). Buzz 47 pollination is by no means rare. The ability to produce vibrations to remove pollen from 48 flowers has evolved at least 45 times in the evolutionary history of bees, and it is estimated 49 that approximately 6% of flowering plants are buzz-pollinated (Cardinal et al., 2018). In most 50 buzz-pollinated plants, pollen is kept locked inside tubular, non-dehiscent anthers (i.e., 51 poricidal anthers; Buchmann, 1983; Harris, 1905), or inside closed corolla tubes with small 52 apical openings (Corbet and Huang, 2014; Kawai and Kudo, 2008; Macior, 1968) that restrict 53 direct access to pollen. Pollen grains in buzz-pollinated flowers are most efficiently removed by 54 bees that are capable of using floral vibrations—also called “sonications” or “buzzes”—to 55 release pollen from poricidal anthers and flowers (De Luca and Vallejo-Marín, 2013). Despite 56 the widespread occurrence of the ability to produce floral vibrations among bees 57 (Hymenoptera: Apoidea: Anthophila), little is known about why some bee species buzz- 58 pollinate (e.g., carpenter bees, bumblebees, several sweat bees), while others seem incapable 59 of doing so (e.g., honeybees and most leaf-cutter bees) (Cardinal et al., 2018; De Luca and 60 Vallejo-Marín, 2013). Moreover, we are still in the early stages of understanding the extent to 61 which floral vibrations produced by bees vary between bee species and between different 62 types of plants. 63 The production of floral vibrations by bees is a relatively stereotyped behaviour (De 64 Luca and Vallejo-Marín, 2013). During a typical buzz-pollinating visit, a bee embraces one or 65 more poricidal anthers, holding to the anthers using its mandibles, curls its body around the 66 anthers, and produces one or more bursts of vibrations that can be heard by a human 67 observer as “buzzes” of a higher pitch than that buzz heard during flight (Macior, 1964; Russell 68 et al., 2016) (Fig. 1). A bee generates floral vibrations using its thoracic musculature, which 69 causes rapid deformation of the thorax while the wings remain undeployed (King and 70 Buchmann, 2003). These vibrations are transmitted as substrate-borne vibrations to the 71 anthers through the mandibles/head, thorax and abdomen of the bee (King, 1993; Vallejo- 72 Marin, in review). The vibrations result in pollen ejection from the anther tips (Fig. 1), probably 73 as a consequence of energy transfer from the bee to the pollen grains (Buchmann and Hurley, 74 1978), which should be a function of the mechanical properties of the substrate-borne 75 vibrations as well as the characteristics of both bee and flower (Vallejo-Marin, in review). 76 Determining exactly what characteristics of floral vibrations are most important for pollen 77 release is an area that requires further theoretical and empirical work. 4 bioRxiv preprint doi: https://doi.org/10.1101/494690; this version posted December 13, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 78 Floral vibrations produced by bees are a type of substrate-borne vibration and can be 79 described by biophysical properties such as duration, frequency and amplitude (Cocroft and 80 Rodríguez, 2005; Mortimer, 2017). During a single visit, a bee may produce one to several 81 “buzzes”, but each of them can be itself made from very short vibrations (tens to hundreds of 82 milliseconds) (Vallejo-Marin, in review) (Fig. 2a), although a single vibration may go 83 uninterrupted for longer (seconds) (Buchmann and Cane, 1989). Floral vibrations contain 84 multiple harmonics (Buchmann et al., 1977), although usually the fundamental frequency (first 85 harmonic) contributes most to the overall magnitude of substrate-borne floral vibrations (De 86 Luca and Vallejo-Marín, 2013; King, 1993). In such cases, the fundamental frequency is also the 87 dominant or peak frequency (Fig. 1). The fundamental frequency of floral vibrations typically 88 ranges between 100 and 500 Hz (De Luca and Vallejo-Marín, 2013). Floral vibrations can also 89 be characterised by their amplitude (Figs. 2b and 2c). Amplitude describes the magnitude of 90 oscillatory movement, and can itself be defined in terms of acceleration, velocity and 91 displacement (Sueur, 2018). In many types of oscillatory movement, frequency, acceleration, 92 velocity and amplitude are interrelated, and a full description of an oscillation thus requires 93 knowledge of the absolute value of more than one of these variables. However, assuming 94 simple harmonic oscillations it is possible to use two of these variables (e.g., frequency and 95 acceleration) to calculate another one (e.g., displacement) (Vallejo-Marin, in review). An 96 approach often taken to characterise floral vibrations during buzz pollination is to use acoustic 97 recordings. Audio recordings provide accurate estimates of some aspects of substrate-borne 98 vibrations, such as frequency and duration, but are less reliable in estimating the amplitude 99 component (De Luca et al., 2018). As floral vibrations are in essence a substrate-borne 100 phenomenon, measurements of the vibrations experienced by flowers thus require the 101 vibrations transmitted to the flowers to be assessed directly using, for example, 102 accelerometers or laser vibrometers (Vallejo-Marin, in review). To date, very few studies have 103 attempted to compare floral vibrations produced by different species of bee visiting different 104 species of plant using direct measurements of substrate-borne vibrations. 105 Our study focuses on bumblebees (Bombus spp. Latreille), which are well-known for 106 their ability to buzz-pollinate and are important buzz-pollinators in both temperate and 107 tropical regions (De Luca et al., 2014; Mesquita-Neto et al., 2018; Rosi-Denadai et al., 2018).
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