Details of statistics are given in Table 3. (A,C,E) Buzzes in the time domain (oscillograms); (B,D,F) buzzes in the frequency domain (frequency spectra). Although, it was previously (2019) and King (1993) calculated after measuring floral buzzing from the plant and correcting with the corresponding coupling factor. Both laser vibrometer and accelerometer data were simultaneously recorded and time-stamped using a data acquisition system (cRIO model 9040 with the C series module NI 9250; National Instruments, Newbury, UK) using a custom-made LabVIEW 2019 (National Instruments) program (see Pritchard and Vallejo-Marin, 2020, with updated version available at https://github.com/davidjamespritchard/BuzzCatcher). The anthers are completely sealed except for a small pore at the top or have very small slits that open along the sides. Maintaining red clover population in New Zealand at the time was critical to the country's crop production rate. "Floral Sonication is an Innate Behaviour in Bumblebees that can be Fine-Tuned with Experience in Manipulating Flowers", "The Economic Impacts of Pollinator Declines: An Approach to Assessing the Consequences", "A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination". 1). 3A; Table 1). In this study we directly compared these different types of vibrations within a single species of bumblebee, not only comparing flight and non-flight vibrations, but also characterising different types of non-flight vibrations. Buzz pollination is by no means rare. The buzzing behaviour that some bees display on flowers to extract pollen has also been called ‘floral sonication’ due to the distinctive sound the vibrations produce. (2) To what extent do floral vibrations produced by the bee depend on the species of flower being visited? 5A; Table 2). But it’s also critical to human agriculture. The neck of the bee was held by a loop of fine nylon string threaded through a needle and attached to a syringe secured by a clamp (Fig. Oscillograms and frequency spectra of vibrations (buzzes) produced by bumblebees (Bombus terrestris audax) in three different behavioural contexts: flight (A,B), defence (C,D) and buzz-pollination (E,F). Buzz‐pollination is performed by female bees (Anthophila) in thousands of species, having evolved at least 45 times within the group (Cardinal, Buchmann, & Russell, 2018). Although it is not clear exactly how costly these floral buzzes might be, as no-one has yet measured the metabolic cost of floral buzzing, it has been suggested that bees work to maximise the efficiency of their pollen collection (Rasheed and Harder, 1997). Among bees, vibrations play a particularly multifaceted role. Does the preferred walk–run transition speed on steep inclines minimize energetic cost, heart rate or neither? In contrast, the fundamental frequency of the floral vibrations was similar whether recorded directly from the bee (313.16±2.86 and 312.09±4.99 Hz for S. rostratum and S. citrullifolium, respectively) or indirectly via the accelerometer on the flower (312.70±2.92 and 313.16±4.81 Hz for S. rostratum and S. citrullifolium, respectively; Fig. These findings suggest that a bee of a given size could adjust its buzz frequency in relation to these or associated floral traits. buzz duration and amplitude on pollen release, the effect of buzz frequency on pollen release remains unclear. Rosi-Denadai CA, Araújo PCS, Campos LAO, Cosme L Jr, Guedes RNC. We found that bumblebees vibrating flowers produce higher accelerations than in other behaviours, and much higher than previously thought. Vibrations play an essential role in the natural behaviour of animals, particularly among invertebrates. How bees handle flowers, where they bite anthers, and how they position themselves as they vibrate, could all influence how the high acceleration vibrations we recorded are applied to the flower and result in pollen ejection. Animal vibrations can be transmitted both through the air (sound) and through the underlying substrate (most often plant tissue) as substrate-borne vibrations (Cocroft and Rodríguez, 2005). Yet recent work indicates that although frequency components are reliably inferred from either acoustic or substrate-borne measurements, the magnitude of substrate-borne vibrations is poorly correlated with the magnitude of their acoustic component (De Luca et al., 2018). For each bee we analysed an average of 6.13 buzzes (N=98 buzzes from 16 bees). The efficiency of this process is directly affected by the mechanical properties of the buzzes, namely the duration, amplitude, and frequency. (A,C,E) Buzzes in the time domain (oscillograms); (B,D,F) buzzes in the frequency domain (frequency spectra). Laser vibrometry provides a direct, contactless measure of the vibrations produced by the bee. In bees, the same mechanism that drives the wings during flight is responsible for producing vibrations used during communication, defence and buzz-pollination. The total profit of this industry has been recorded to produce over €111 million a year, with €61 million coming in from bumblebees alone. Traditionally, pollination has been done by shaking using electric vibrators (one brand name was "Electric Bee"), however, it has been found to be less expensive in human labor and plant breakage to use bumblebees within the greenhouses. Moreover, the relationship between the frequency of floral buzzes and bee size within species may further depend on the metric of bee size used (Corbet and Huang, 2014; Switzer and Combes, 2017). 2019). 3C). Azaleas and rhodendrons need to get buzzed, and so do certain legumes like partridge pea, a beautiful wildflower found in … The flower morphology of buzz pollinated plants is different from other flora that do not use this type of pollination. By using lower frequency and velocity vibrations, bumblebees might be able to perform defence buzzes for longer, increasing their effectiveness against predators. To get a more complete view of how vibrations differ across bee behaviours, it is necessary to capture both frequency and amplitude components (Vallejo-Marín, 2019). NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. Background and aims: Buzz pollination involves explosive pollen release in response to vibration, usually by bees. audax (Harris 1776); hereafter B. audax] both during flight and in two different non-flight behavioural contexts: defence and floral vibrations. Peak amplitude velocity and fundamental frequency of floral buzzes of B. audax on buzz-pollinated flowers of Solanum rostratum and S. citrullifolium. After returning to room temperature, bees resumed normal activity after approximately 7–10 min and were released back into the colony. We thank all members of the Vallejo-Marín Laboratory, particularly Carlos Eduardo Pereira-Nunes and Jurene Kemp, for their help with bee maintenance and useful conversations about buzz pollination, and Shoko Sugasawa for comments on the manuscript. Vibrations recorded on the flower had significantly lower peak velocities but similar fundamental frequencies to those measured in the bee. If floral buzzing exerts a significant cost on bees, this cost might play an important role in their decisions about where and when to forage on buzz-pollinated flowers (Stephens, 2008). This is could be an evolutionary strategy to prevent self-fertilization, also known as selfing, by creating distance between the stigma.[4]. (C) Relationship between bee size (intertegular distance) and the fundamental frequency of floral buzzes; each symbol in represents the average frequency from multiple buzzes produced by an individual bee. The mechanism of pollen release is poorly understood, and it is not clear which component of vibration (acceleration, frequency, displacement or velocity) is critical; the role of buzz frequency has been particularly controversial. The ability to produce vibrations to remove pollen from flowers has evolved at least 45 times in the evolutionary history of bees, and it is estimated that approximately 6%offlowering plants are buzz pollinated (Cardinal et al., 2018). The calibrated shaker produces a vibration of constant properties (frequency=159.2 Hz, RMS amplitude velocity=9.8 mm s−1) that are transmitted to a small metal plate at one end of the instrument. By increasing frequency and amplitude velocity and acceleration of their vibrations during vibratory pollen collection, foraging bees may be able to maximise pollen removal from flowers, although their foraging decisions are likely to be influenced by the presumably high cost of producing floral vibrations. Artificial vibrations between 450 and 1000 Hz remove twice as much pollen than vibrations of 400 Hz (Harder & Barclay, 1994 ). Vibrations measured with the laser were sampled at a rate of 10,240 Hz using a low pass filter of 5 Hz, and a maximum velocity range of either 100 mm s−1 (for bees 1–14) or 500 mm s−1 (for bees 15–32). This wasn’t always the case. as sound) (Barth et al., 2005; Cocroft and Rodríguez, 2005; Mortimer, 2017). However, within the range of frequencies produced by some bumblebees (240-405 Hz), frequency has a modest effect on pollen release (De Lucaet al., 2013). Despite its prevalence in pollination systems, the ecological and evolutionary conditions that favour the evolution of buzz-pollination are poorly known. Only a few insect species are able to pollinate these plants. [8] The relationship between buzz pollinated plants and bees benefits both groups and could be why poricidal anthers have been successful evolutionarily. Vibrations differed in both peak velocity (A) and frequency (B), with floral buzzes exhibiting the highest velocity and highest frequency buzzes, and flight producing the lowest velocity and frequency vibrations. We do not capture any email address. A full characterisation of substrate-borne vibrations is particularly important in the context of buzz-pollination because biophysical models of poricidal anthers (Buchmann and Hurley, 1978), as well experimental tests with artificial buzzes, suggest that vibration amplitude, rather than frequency, is a key determinant of the rate of pollen ejection from flowers (De Luca et al., 2013; Rosi-Denadai et al., 2018). 5B; Table 2). In bumblebees (Bombus spp. Traditionally, substrate-borne vibrations produced by bees have been studied indirectly by recording the air-borne component of the vibration using acoustic recorders. For defence and flight buzzes (B,C), bees were tethered to a platform using a nylon wire loop fed through a blunted needle. The following plants are pollinated more efficiently by buzz pollination: The earliest evidence of ancestors of plants that use this mode of pollination in the fossil record has been dated to the Cretaceous period. During flight, both the dorsoventral and dorsal longitudinal muscle sets are stimulated equally, whereas during defensive buzzes the dorsal longitudinal muscles are stimulated at twice the rate of the dorsoventral muscles (King et al., 1996). Buchmann and Cane, 1989; King and Buchmann, 1996), and S. rostratum and S. citrullifolium have been directly compared in a previous study that identified differences in the coupling factors of these species (Arroyo-Correa et al., 2019). To stimulate flight (C), the platform was rapidly lowered, triggering reflexive flight. We found no statistically significant interaction between bee size and plant species on either frequency or peak amplitude velocity of floral vibrations. By identifying homologous mechanisms as well as outlining possible constraints on how insect vibrations respond to selection, investigating the mechanisms of bumblebee vibrations can also tell us more about how these behaviours evolve. Nesting behavior and bionomics of a solitary ground-nesting wasp, Buzz-pollination in Neotropical bees: genus-dependent frequencies and lack of optimal frequency for pollen release, Receiver psychology and the evolution of multicomponent signals, Bees learn preferences for plant species that offer only pollen as a reward, Concealed floral rewards and the role of experience in floral sonication by bees, Fiji: an open-source platform for biological-image analysis, Decision ecology: foraging and the ecology of animal decision making, Seewave: a free modular tool for sound analysis and synthesis, Bumblebee sonication behavior changes with plant species and environmental conditions, Sonicating bees demonstrate flexible pollen extraction without instrumental learning, Phylogenetic clustering of wingbeat frequency and flight-associated morphometrics across insect orders, Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen, (ed. These vibrations cause pollen (carrying the plant’s male gametes) to bounce inside the anthers and eventually be forcefully propelled outside the anther and onto the … In addition to considering differences in the actions of the muscles, another approach to thinking about why the muscles produce vibrations with these particular properties is to consider what properties might best serve these functions. Although the bees did not know the O. frutescens would benefit from these multiple visits as the plants continue to produce pollen during the flowering season. The accelerometer was attached to the calyx at the base of the flower being vibrated by the bee using a 5 mm×0.35 mm pin made from an entomological pin (Austerlitz black enameled size 0, Entomoravia, Slavkov u Brna, Czech Republic) and glued to the accelerometer with instant adhesive as described by Arroyo-Correa et al. In addition to producing vibrations during locomotion and as a signal to predators or conspecifics, the two forms of thoracic vibrations most commonly studied in bees and other insects, buzz-pollinating bees also use vibrations to forage. In panels A and B, values are means±s.e.m. Enter multiple addresses on separate lines or separate them with commas. To quantify the extent to which the vibrations produced by bees differ from those measured in the flower itself, we calculated King's coupling factor (King, 1993). This vibration causes the pollen to become dislodged from the anther and onto the bee. Pollen contains a substantial amount of protein compared to nectar, the sugary liquid the majority of plants produce as a reward for their animal pollinators. In contrast, the peak amplitude displacement of floral (0.27±0.009 mm) and defence buzzes (0.27±0.007 mm) were similar, although both were greater than the displacement amplitude of flight vibrations (0.14±0.005 mm) (Fig. Each colony had access to ad libitum ‘nectar’ solution (1 M sucrose solution) within the colony. The ability to use vibrations during pollen harvesting occurs in approximately 58% of all bee (Anthophila) species including 15% of genera in all bee families (Cardinal et al., 2018), and buzz-pollination (pollination using vibrations) is associated with more than 20,000 species of flowering plants (Buchmann, 1983; De Luca and Vallejo-Marín, 2013). Currently the mechanisms that control the properties of thoracic vibrations have only been studied in a handful of contexts (Esch and Goller, 1991; King et al., 1996), with most of what we know coming from studies of flight control in Drosophila (Lehmann and Bartussek, 2017; Lindsay et al., 2017). Rather than just comparing flight and non-flight vibrations, we used accelerometers and laser vibrometry to directly measure the vibrational properties of buzzes produced by bumblebees [Bombus terrestris ssp. Finally, to compare the effect of flower species and recording method on coupling factors, we used a linear mixed effect model with coupling factor as a response variable, flower species, ITD and vibration method (bee vs artificial) as explanatory variables, and bee identity as a random effect. The fundamental buzz frequencies in buzz-pollination typically range from 100 to 400 Hz (Burkart et al., 2011; De Luca & Vallejo-Mar´ın, 2013). Details of statistics are given in Table 1. To induce defence buzzes, the tethered bees were gently squeezed along the sides using featherweight forceps. Over 50 genera of bees release pollen from flower anthers using thoracic vibrations, a phenomenon known as buzz‐pollination. The floral vibrations measured in this experiment were on average 500 m s−2, more than two to three times what Arroyo-Correa et al. Details of statistics are given in Table 2. [4] The stigmas of these flowers are often located below the anthers. Although within nar-row ranges such frequencies may not be distinguishable The next step for understanding why bumblebees, and other insects, produce the vibrations they do, is to understand how other behaviours work alongside vibrations to serve their function. Buchmann, S. J. Kansas Entomol. Our results show clear differences in biomechanical properties of defence and floral buzzing, as well as differences between these vibrations and those produced during flight. The authors declare no competing or financial interests. Experimental set-up for measuring bee vibrations. Floral buzzes also had significantly higher frequencies (313.09±2.63 Hz) than both defence (236.32±4.29 Hz) and flight buzzes (136.95±1.73 Hz) (Fig. To compare the properties of floral vibrations on different Solanum species, we employed linear mixed effect models, using either laser-recorded peak velocity, laser-recorded fundamental frequency, accelerometer-recorded peak velocity or accelerometer-recorded fundamental frequency as response variables, flower species and ITD as explanatory variables, and bee identity as a random effect. After 7–10 min, the tethered bee had returned to regular activity levels and we continued with data collection. Buzz-pollination is probably an innate behaviour in some species, as naive Bombus terrestris bumblebees foraging on buzz-pollinated flowers will exhibit buzzing on their first foraging trips . Most studies of insect vibrations have focused on vibrations produced for communication or as a by-product of flight (Tercel et al., 2018; Hill et al., 2019). While wing deployment can explain the difference between flight and non-flight vibrations, it cannot explain the differences between the two non-flight vibrations (floral and defence buzzes), where the wings remained folded and the mass of the system remains unchanged. Following recording, tethered bees were immobilised again by being placed in the freezer, removed from the tether, placed in a plastic container, and euthanised in the −26°C freezer. The key question raised by our results, then, is why are the properties of floral, defence and flight vibrations so different from one another? Unlike defence buzzes, the primary function of floral buzzes is not to transmit information to receivers but to shake pollen loose from flowers. Greenewalt, 1962; Joos et al., 1991). Vibrations applied to S. rostratum show less attenuation than vibrations applied to S. citrullifolium, making this pair an ideal comparison for the effect of bee-produced vibrations on flowers. A. Dafni, M. Hesse and E. Pacini, E.), Buzz pollination: studying bee vibrations on flowers, Recurrent modification of floral morphology in heterantherous, Calcium and stretch activation modulate power generation in, Pollen in bee-flower relations some considerations on melittophily. The biomechanical properties of a vibration might only be part of what makes it effective. As with velocity, we analysed the peak recordings of each of these measures with linear mixed effect models, with buzz type and ITD as explanatory variables and bee identity as a random effect. Bumblebees and other buzz-pollinating bees present a unique opportunity for research on insect vibrations. In contrast, bee size was negatively associated with frequency of floral and flight buzzes, but positively with defence buzzes. These experiments were approved by the Animal Welfare and Ethical Review Board of the University of Stirling. Monica has had a long association with JEB before taking up her new role, overseeing peer review of neuromuscular physiology, terrestrial biomechanics and integrative physiology of locomotion. Buzz pollination takes its name from the audible component, or ‘buzz’, that can be heard when a bee vibrates a flower (Macior, 1964). Analysis of bee size (intertegular distance), plant species and recording location on the properties of floral vibrations. (2008). However, in North America, the managed honeybee industry experienced decline in the early 2000s due to colony collapse disorder. The pores and slits are small enough that insects cannot easily enter the anther, but large enough pollen can exit. [9], One of the most common plants that are assisted by buzz pollination is the tomato (Lycopersicon esculentum). We also detected an interaction between bee size and buzz type, with larger bees achieving higher frequency defence buzzes and lower frequency flower and flight buzzes than smaller bees (Table 2, Fig. Explaining that this process is known as ‘buzz pollination’, Vallejo-Marín adds that more than 20,000 plants have to be shaken like a pepper pot to distribute their pollen, while half of all bees tremble flowers to extract the nutritious grains. The coloured section in the oscillograms shown in panels A and C represent the section of the buzz used to calculate the frequency spectra shown in panels B and D. The dashed lines in panels B and D represent the first five harmonics of the fundamental frequency. The frequency of flight vibrations in bees is usually negatively associated with size both within (this study) and across species (De Luca et al., 2019). Out comes the pollen in a spew. For each flower, we selected one clean recording, converted voltage to velocity as described above, and obtained King's coupling factor for the shaker (Kshaker) using the ratio between expected and observed RMS velocity. Most buzz-pollinated flowers keep pollen tightly locked inside their anthers and the only efficient way to extract it is through animal vibrations. For the recording of flight and defence buzzes, bees were selected at random from the flight box. Body size is expected to affect frequency as a … Rosi-Denadai et al. Similar factors could influence the ‘best’ properties for defence buzzes. For each bee, we analysed an average of 5.6 flight vibrations (N=112 vibrations from 20 bees) and 6.8 defence buzzes (N=136 from 20 bees). Buzz-pollination in Neotropical bees: genus-dependent frequencies and lack of optimal frequency for pollen release. Conceptualization: D.J.P., M.V.-M.; Methodology: D.J.P., M.V.-M.; Software: D.J.P. Differences in the properties of vibrations (buzzes) produced in different contexts (flight, defence and floral buzzes). Between the two studied plant species, we found that Solanum rostratum is better at transmitting vibrations applied on the anthers to other parts of the flower than S. citrullifolium, as shown by its lower coupling factor (cf. These vibrations cause pollen (carrying the plant’s male gametes) to bounce inside the anthers and eventually be forcefully propelled outside the anther and onto the … Although in our experiment we found that defence buzzes were on average of lower frequency, peak amplitude velocity and peak amplitude acceleration than floral buzzes, these properties do not correlate with what is likely a more important property of a warning signal: volume (De Luca et al., 2018). Producing high acceleration floral buzzes, however, is likely to have come with a cost. Biotremology: do physical constraints limit the propagation of vibrational information? It is possible that the properties of floral buzzes are also tuned to maximise the pollen collected from poricidal anthers. Because of this shape, they are often referred to as poricidal anthers. For defence buzzes (B), bees were gently squeezed on the abdomen using featherweight tweezers. Our analysis showed no difference within plant species between coupling factors calculated from either bee floral buzzes (Kbee) or synthetic vibrations applied with the calibrated shaker (Kshaker) (Table 3), although Kbee is less variable than Kshaker (Fig. 6). A lower frequency and velocity vibration may also be beneficial for the bee as it might be less energetically costly than the higher frequency and velocity floral buzz. We used two colonies of the buff-tailed bumblebee, Bombus terrestris audax (Biobest, supplied by Agralan Ltd, Swindon, UK). Although, it was previously Only a few insect species are able to pollinate these plants. [2] About 9% of the flowers of the world are primarily pollinated using buzz pollination. The metal plate of the calibrated shaker was firmly pushed against the feeding anthers of the flower, and we recorded four to five samples of 2 s each using the data acquisition system described above (see ‘Analysing vibrations’ section). Professor Fernando Montealegre-Z (University of Lincoln) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. Unlike some other Solanum species, S. rostratum and S. citrullifolium are both heterantherous, with bees primarily focusing their attention on ‘feeding anthers’ presented at the centre of the flower, while a single, rarely visited ‘pollinating anther’ deposits pollen on the visiting bee. We found little evidence that the magnitude of floral, flight and defence buzzes can be explained by the range of bee size variation observed within a single species of bumblebee. All analyses were performed using lme4 (Bates et al., 2015) to estimate parameters and lmerTest (Kuznetsova et al., 2017) to assess statistical significance. [11] In Australia, as bumblebees are not native, and Australia has a number of widely publicised environmental disasters caused by escaped introduced species ("feral species"), research is under way to adapt the use of the Australian native Amegilla cingulata (blue banded bees) for the same task. Specifically, we explored how body size influences the frequency of buzz-pollination vibrations. 5C), while bee size had no effect on their peak amplitude velocity (Table 2). In addition to peak velocity and frequency, which were measured directly, we also used these measures to derive the displacement amplitude (in mm) and acceleration (in mm s−2) of the vibration.

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