Variation in plant leaf traits affects transmission and detectability of herbivore vibrational cues

Velilla, Estefania; Polajnar, Jernej; Virant-Doberlet, Meta; Commandeur, Daniël; Simon, Ralph; Cornelissen, Johannes H. C.; Ellers, Jacintha; Halfwerk, Wouter

doi:10.1002/ece3.6857

Cited by 14 publications

(9 citation statements)

References 60 publications

(93 reference statements)

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“…However, other morphological differences between the four species are also likely to be important in determining vibration transmission. Studies on other types of insect vibrations have shown that flexible plant stems attenuate vibrations more than stiff stems, as do thick leaves compared with thin leaves 4 , 5 . In buzz-pollinated flowers, traits affecting vibration properties might include anther curvature (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Insects use substrate-borne vibrations in a range of ecological contexts, including conspecific communication and the detection of prey and predators 1 , 2 . These vibrations are often produced and detected on plant material, and the physical properties of the plant substrate, such as stem stiffness or leaf thickness, often affect vibration propagation 3 – 5 . Approximately 6–8% of angiosperms are buzz-pollinated, relying on substrate-borne vibrations (floral buzzing), typically produced by bees, to release pollen from flowers with specialised morphologies 6 , 7 .…”

Section: Introductionmentioning

confidence: 99%

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Transmission of bee-like vibrations in buzz-pollinated plants with different stamen architectures

Nevard

Russell

Foord

et al. 2021

Sci Rep

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In buzz-pollinated plants, bees apply thoracic vibrations to the flower, causing pollen release from anthers, often through apical pores. Bees grasp one or more anthers with their mandibles, and vibrations are transmitted to this focal anther(s), adjacent anthers, and the whole flower. Pollen release depends on anther vibration, and thus it should be affected by vibration transmission through flowers with distinct morphologies, as found among buzz-pollinated taxa. We compare vibration transmission between focal and non-focal anthers in four species with contrasting stamen architectures: Cyclamen persicum, Exacum affine, Solanum dulcamara and S. houstonii. We used a mechanical transducer to apply bee-like vibrations to focal anthers, measuring the vibration frequency and displacement amplitude at focal and non-focal anther tips simultaneously using high-speed video analysis (6000 frames per second). In flowers in which anthers are tightly arranged (C. persicum and S. dulcamara), vibrations in focal and non-focal anthers are indistinguishable in both frequency and displacement amplitude. In contrast, flowers with loosely arranged anthers (E. affine) including those with differentiated stamens (heterantherous S. houstonii), show the same frequency but higher displacement amplitude in non-focal anthers compared to focal anthers. We suggest that stamen architecture modulates vibration transmission, potentially affecting pollen release and bee behaviour.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transmission of bee-like vibrations in buzz-pollinated plants with different stamen architectures

Nevard

Russell

Foord

et al. 2021

Sci Rep

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“…In addition to increasing the velocity of thoracic vibrations as described above, bees have other behavioural tools at their disposal to increase anther velocity during buzz pollination. The capacity to shake floral structures depends not only on the vibrations produced by the bee’s thorax but also on the characteristics of the flower and on the bee–flower coupling ( King, 1993 ; Arroyo-Correa et al , 2019 ; de Langre, 2019 ; Switzer et al , 2019 ; Vallejo-Marín, 2019 ; Velilla et al , 2020 ; Timerman and Barrett, 2021 ). Bees may benefit from selecting to visit flowers in which they may impose higher accelerations to the anthers and thus increase the rate of pollen removal (e.g.…”

Section: Implications For Buzz Pollinationmentioning

confidence: 99%

How and why do bees buzz? Implications for buzz pollination

Vallejo‐Marín

2021

Journal of Experimental Botany

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Buzz pollination encompasses the evolutionary convergence of specialised floral morphologies and pollinator behaviour in which bees use vibrations (floral buzzes) to remove pollen. Floral buzzes are one of several types of vibrations produced by bees using their thoracic muscles. Here I review how bees can produce these different types of vibrations and discuss the implications of this mechanistic understanding for buzz pollination. I propose that bee buzzes can be categorised according to their mode of production and deployment into: (1) thermogenic, which generate heat with little mechanical vibration; (2) flight buzzes, which combined with wing deployment and thoracic vibration, power flight, and (3) non-flight buzzes in which the thorax vibrates but the wings remain folded, and include floral, defence, mating, communication, and nest-building buzzes. I hypothesise that the characteristics of non-flight buzzes, including floral buzzes, can be modulated by bees via modification of the biomechanical properties of the thorax through activity of auxiliary muscles, changing the rate of activation of the indirect flight muscles, and modifying flower handling behaviours. Thus, bees should be able to fine-tune mechanical properties of their floral vibrations, including frequency and amplitude, depending on flower characteristics and pollen availability to optimise energy use and pollen collection.

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“…However, other morphological differences between the four species are also likely to be important in determining vibration transmission. Studies on other types of insect vibrations have shown that flexible plant stems attenuate vibrations more than stiff stems, as do thick leaves compared with thin leaves (Cocroft et al, 2006;Velilla et al, 2020). In buzz-pollinated flower, traits affecting vibration properties might include anther curvature (e.g.…”

Section: Transmission Of Vibrationsmentioning

confidence: 99%

“…Insects use substrate-borne vibrations in a range of ecological contexts, including conspecific communication and the detection of prey and predators (Cocroft and Rodríguez, 2005;Mortimer, 2017). These vibrations are often produced and detected on plant material, and the physical properties of the plant substrate, such as stem stiffness or leaf thickness, often affect vibration propagation (Cocroft et al, 2006;Kollasch et al, 2020;Velilla et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Transmission of vibrations in buzz-pollinated plant species with disparate floral morphologies

Nevard

Russell

Foord

et al. 2021

Preprint

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In buzz-pollinated plants, bees apply vibrations produced by their thoracic muscles to the flower, causing pollen release from anthers, often through small apical pores. During floral buzzing, bees grasp one or more anthers with their mandibles, and vibrations are transmitted to the focal anther(s), adjacent anthers, and the whole flower. Because pollen release depends on the vibrations experienced by the anther, the transmission of vibrations through flowers with different morphologies may determine patterns of release, affecting both bee foraging and plant fitness. Anther morphology and intra-floral arrangement varies widely among buzz-pollinated plants. Here, we compare the transmission of vibrations among focal and non-focal anthers in four species with contrasting anther morphologies: Cyclamen persicum (Primulaceae), Exacum affine (Gentianaceae), Solanum dulcamara and S. houstonii (Solanaceae). We used a mechanical transducer to apply bee-like artificial vibrations to focal anthers, and simultaneously measured the vibration frequency and displacement amplitude at the tips of focal and non-focal anthers using high-speed video analysis (6,000 frames per second). In flowers in which anthers are tightly held together (C. persicum and S. dulcamara), vibrations in focal and non-focal anthers are indistinguishable in both frequency and displacement amplitude. In contrast, flowers with loosely arranged anthers (E. affine) including those in which stamens are morphologically differentiated within the same flower (heterantherous S. houstonii), show the same frequency but higher displacement amplitude in non-focal anthers compared to focal anthers. Our results suggest that stamen arrangement affects vibration transmission with potential consequences for pollen release and bee behaviour.

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Variation in plant leaf traits affects transmission and detectability of herbivore vibrational cues

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 14 publications

References 60 publications

Transmission of bee-like vibrations in buzz-pollinated plants with different stamen architectures

Transmission of bee-like vibrations in buzz-pollinated plants with different stamen architectures

How and why do bees buzz? Implications for buzz pollination

Transmission of vibrations in buzz-pollinated plant species with disparate floral morphologies

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