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Journal of Experimental Botany, Vol. 73, No. 4 pp. 1063–1066, 2022 https://doi.org/10.1093/jxb/erac007 This paper is available online free of all access charges (see https://academic.oup.com/jxb/pages/openaccess for further details) eXtra Botany Special Issue Editorial New insights and opportunities from taking a biomechanical perspective on plant ecology Downloaded from https://academic.oup.com/jxb/article/73/4/1063/6535205 by guest on 28 June 2022 Mechanical ecology is an emerging interdisciplinary field approach: the very promising and timely fusion of biomech- at the intersection of biomechanics and field ecology. anics and ecology (Box 1). The development of ever smaller and more powerful port- Biomechanics is an engineering–mathematics-based ap- able devices for measurement and data acquisition has proach to understanding biological questions and processes boosted the number of biomechanical field studies in re- (Vogel, 1988). It has its roots in zoological, biomedical, and cent years, shedding new light on often neglected, but sports science, but the impact and popularity of plant biomech- crucial factors influencing mechanical aspects of plant anics is rapidly growing. This is evidenced by the emergence ecology. This Special Issue showcases recent scientific of several dedicated conferences (e.g. the International Plant and technological advances, and highlights the import- Biomechanics Conference), and by multiple special issues in ance of considering the mechanical aspects of plant journals, including two in JXB over the past decade (in 2019, ecology, as well as putting biomechanical mechanisms Plant Biomechanics: Force, Form, and Function; and in 2013, into a biologically relevant real-world context. Plant Biomechanics and Mechanobiology). Plant ecology, however, is traditionally looking towards chemistry and physi- ology to explain responses of plants to biotic and abiotic stress ‘there is an underlying world with which life must factors, and climate change research focuses largely on the ef- contend’ fects of rising temperature, increasing frequency and severity Steven Vogel (1988) of droughts, elevated CO2 availability, and decreasing soil fer- All matter, including life on Earth, is subject to the rules tility on natural vegetation and agricultural crops (Pareek et of physics. Physical forces govern processes at all scales from al., 2020). Mechanical aspects of plant ecology thus remain atoms to ecosystems, and considering these forces is essential poorly studied to date, and plant biomechanics is still largely for a comprehensive understanding of plant ecology and evo- confined to the lab; however, the key to fully understanding lution (Box 1). For example, the increasing frequency of se- the impact of mechanical factors is to research them in the vere weather events as a result of global climate change leads field, under natural conditions (Bauer et al., 2020; Niklas and to ever higher mechanical stresses on plants and the soil that Telewski, 2022). supports them (Ummenhofer and Meehl, 2017; Rädler et al., From the obvious (e.g. wind, waves, and impacts from rain 2019), but how plants cope with such dramatic changes, which and hail) to the more obscure (e.g. gravitational and electro- mainly occur in evolutionarily irrelevant time scales, is largely static forces, and microvibrations), mechanical factors affect unknown (e.g. Onoda et al., 2010; Heredia-Guerrero et al., virtually every aspect of plant life (Read and Stokes, 2006). In 2018; Johnson et al., 2019). Mitigating the immediate effects this issue, Niklas and Telewski (2022) explore how mechanical of these extreme weather events therefore requires an integra- constraints and trade-offs played a key role in shaping modern tive understanding of the physical factors influencing natural plants as they transitioned from marine to terrestrial environ- vegetation and crops in order to understand plant responses to ments and colonized the vertical growth space, competing for increasing mechanical stresses, but also the potential of plants light. They show how plant material properties and growth re- to mitigate the effects of climate change-induced alterations of sponses to mechanical loading evolved over time to allow them weather patterns.The unprecedented challenges of our time— to grow taller and resist increasing mechanical loads; however, climate change, habitat and biodiversity loss, food security for a increasing height comes with additional challenges for water growing world population, and accelerating loss of arable soils transport which may conflict with the demands for structural to erosion—require increasingly innovative and interdiscip- reinforcement (Baer et al., 2021). Lianas, epiphytes, and epi- linary approaches to solve (Glamann et al., 2017; Middendorf et parasites circumvent this conflict by largely foregoing structural al., 2020).This Special Issue explores one such interdisciplinary reinforcement and instead relying on other plants for vertical © The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
1064 | Special Issue Editorial support; here, the crucial mechanical adaptations are for secure Box 1. attachment to the host tree, as shown for passionflowers and A multitude of physical forces act upon plants, and the mistletoes in this issue (Klimm et al., 2022; Mylo et al., 2022). resulting mechanical stresses have shaped both the Attachment (or lack thereof) is also crucial for plant–in- overall growth forms and the composite cellular materials sect interactions such as plant carnivory, herbivory, and pol- of extant plant species. Stems and branches must be lination (Whitney and Federle, 2013). Mechanical factors strong enough to resist bending and buckling under the control the timing of pollen release (Nelson et al., 2012; plant’s own load. Moreover, wind gusts and waves shock- Timerman and Barrett, 2021; Vallejo-Marin, 2022) and, load plants with extremely high forces that can cause very recently, the act of pollination itself has been shown catastrophic breakage or uprooting. The impact forces to rely on attractive forces between flowers and bees with of raindrops and hailstones may appear insignificant opposing electrostatic charges—prompting the launch of the in comparison; however, their effect is amplified by subfield of electrical ecology (England and Robert, 2021). Downloaded from https://academic.oup.com/jxb/article/73/4/1063/6535205 by guest on 28 June 2022 the concentration of force on a very small area, as is Electrostatic charges not only promote the movement of demonstrated by the erosive power of rain. Waves pollen between flower and bee, they also function as adver- and tides both cause strong cyclic loading in opposite tising signals alongside colour and scent. While the discovery directions, while rain and hail impacts cause characteristic of electroreception in bees changed our way of thinking damped oscillations of the affected plant part. about pollination in recent years, the mounting evidence However, mechanical forces not only pose the risk of of sound perception in plants may well cause similar ripple tissue damage; they can also contain valuable information, effects in the near future (Khait et al., 2019). That plants and plants have evolved a multitude of mechanosensory can sense gravity has long been known and is evident from structures and mechanisms to exploit this information gravitropic growth responses (Moulia and Fournier, 2009; source. A growing body of evidence shows that plants sense Bérut et al., 2018; Sierra-de-Grado et al., 2022). In this issue, mechanical stresses in expanding cells walls and integrate Gallep and Robert (2022) move on to challenge our under- this information with other factors such as morphogen standing of the regulation of circadian rhythms by linking gradients to establish polarity in developing tissues them to fluctuations of gravitational forces as a result of the and coordinate cell divisions and organ differentiation. lunisolar tide cycles. Microvibrations caused by the chewing mandibles of insects With regard to our initial focus on increasing mechanical alert plants of herbivore attacks and kick-start biochemical stresses as a result of changing climate and weather patterns, defence pathways. Electrostatic forces not only function as the most obvious mechanical demand for plants is damage re- signals for pollinators, but have also been shown to directly sistance to the forces of hail, wind (Gardiner et al., 2016), and aid pollen transfer between flower and bee. waves (Koehl, 2022). Several articles in this issue explore the response of leaves to mechanical loading and impacts. Mimi Koehl (2022) provides a comprehensive overview of the adap- tations and responses of marine macroalgae and seagrasses to the extreme mechanical loads in their wave-swept habitats. Burnett and Gaylord (2022) complement this ecological per- spective with a more technical viewpoint on the frameworks, methodologies, and challenges of measuring wave forces and exposure in the field. Moving to terrestrial ecosystems, Langer et al. (2022) investigated the detailed responses of petiole, lamina, and the interjacent transition zone of peltate Pilea piperomioides leaves to wind loading in unprecedented detail. Interestingly, they found clear differences in the biomechan- ical properties of each component, but no adaptive plasticity in the form of thigmomorphogenetic acclimations in response to prolonged wind exposure. Lauderbaugh and Holder (2022) and Roth-Nebelsick et al. (2022) both apply a biomechanics approach to the detailed characterization of leaf responses to rain drop impacts, while Lenz et al. (2022) integrate the bio- mechanical interaction of leaves with rain into the broader ecological and physiological context. They add to previous calls for performing biomechanical measurements on natur- ally growing plants in the field (Bauer et al., 2020), pointing out the shortcomings of purely correlative field studies on the one hand, and of the extrapolation of lab results to the
Special Issue Editorial | 1065 field on the other hand. Taking biomechanical measurements Ulrike Bauer1,∗, and Simon Poppinga2,∗ out into the field is undoubtedly challenging, but modern ad- 1 vances in measurement technology open up unprecedented School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK opportunities. New low-cost instrumentation and fully cus- 2 Botanical Garden, Technical University of Darmstadt, Department tomizable modular set-ups allow autonomous data collection of Biology, Schnittspahnstraße 2, D-64287 Darmstadt, Germany in the field, often over extended periods of time (Kwok, 2017; Oellermann et al., 2021, Preprint; Burnett and Gaylord, 2022). ∗Correspondence: ulrike.bauer@bristol.ac.uk or simon.poppinga@ Almost ironically, the pioneers of ‘field biomechanics’ were tu-darmstadt.de often marine biologists, despite the sea and the tidal zones being undoubtedly amongst the most challenging environ- References ments to which one could take measurement electronics (Bell Baer AB, Fickle JC, Medina J, Robles C, Pratt RB, Jacobsen AL. and Denny, 1994). 2021. Xylem biomechanics, water storage, and density within roots and shoots of an angiosperm tree species. Journal of Experimental Botany 72, Downloaded from https://academic.oup.com/jxb/article/73/4/1063/6535205 by guest on 28 June 2022 If we master the challenges of combining experimental 7984–7997. and theoretical approaches from engineering and physics Bauer U, Poppinga S, Müller UK. 2020. Mechanical ecology—taking bio- with ecological field experiments, we will not only have a mechanics to the field. Integrative and Comparative Biology 60, 820–828. real chance to improve our understanding of the physical Bell EC, Denny MW. 1994. Quantifying ‘wave exposure‘: a simple device demands on plants and their adaptive responses to these de- for recording maximum velocity and results of its use at several field sites. Journal of Experimental Marine Biology and Ecology 181, 9–29. mands (Niklas and Telewski, 2022), but we might even be able Bérut A, Chauvet F, Legué V, Moulia B, Pouliquen O, Forterre Y. 2018. to tap into plants’ potential to mitigate the effects of climate Gravisensors in plant cells behave like an active granular liquid. Proceedings change and tackle the great challenges of the 21st century. of the National Academy of Sciences, USA 115, 5123–5128. Understanding how plants interact with wind, waves, and Burnett NP, Gaylord B. 2022. Flow, form, and force: methods and frame- precipitation can inform forestry planning and programmes works for field studies of macroalgal biomechanics. Journal of Experimental Botany 73, 1122–1138. aimed at preventing or limiting erosion and stabilizing coast- Denny M. 2021. Wave-energy dissipation: seaweeds and marine plants are lines in times of rising sea levels and more frequent storm ecosystem engineers. Fluids 6, 151. surges (Denny, 2021). Elucidating the mechanical resilience of England SJ, Robert D. 2022. The ecology of electricity and electrorecep- plants to damage from abiotic impacts (hail, rain, and wind) or tion. Biological Reviews 97, 383–413. doi: 10.1111/brv.12804. herbivore and pathogen attacks can inform crop breeders of Gallep CM, Robert D. 2022. Are cyclic plant and animal behaviours driven traits to select for, eventually creating more resilient crops that by gravimetric mechanical forces? Journal of Experimental Botany 73, 1093–1103. produce higher yields and need fewer pesticides. A more com- Gardiner B, Berry P, Moulia B. 2016. Wind impacts on plant growth, prehensive understanding of the factors underlying plant–in- mechanics and damage. Plant Science 245, 94–118. sect interactions can help to conserve pollinator networks and Glamann J, Hanspach J, Abson DJ, Collier N, Fischer J. 2017. predict challenges for vegetation regeneration due to effects of The intersection of food security and biodiversity conservation: a review. climate change and anthropogenic disturbance on pollination Regional Environmental Change 17, 1303–1313. and seed dispersal. Heredia-Guerrero JA, Guzman-Puyol S, Benítez JJ, Athanassiou A, Heredia A, Domínguez E. 2018. Plant cuticle under global change: bio- Seeing the growing scientific interest in mechanical ecology physical implications. Global Change Biology 24, 2749–2751. on both sides of the Atlantic and the breadth of research and Johnson SD, Ryalls JMW, Barton CVM, Tjoelker MG, Wright IJ, topics leaves us with a ‘buzz’—an excited anticipation of things Moore BD. 2019. Climate warming and plant biomechanical defences: to come over the next decade. Mechanical ecology in the silicon addition contributes to herbivore suppression in a pasture grass. Functional Ecology 33, 587–596. sense of field biomechanics truly feels like an interdisciplinary Khait I, Obolski U, Yovel Y, Hadany L. 2019. Sound perception in plants. field on the cusp of fully taking off. This Special Issue, along Seminars in Cell and Developmental Biology 92, 134–138. with dedicated conference sessions at the most recent SICB Klimm F, Schmier S, Bohn HF, Kleiser S, Thielen M, Speck T. 2022. (2022: S10 Integrating ecology and biomechanics to investi- Biomechanics of tendrils and adhesive pads of the climbing passion flower gate patterns of phenotypic diversity: evolution, development, Passiflora discophora. Journal of Experimental Botany 73, 1190–1203. and functional traits) and upcoming SEB (2022: Mechanical Koehl MAR. 2022. Ecological biomechanics of marine macrophytes. Journal of Experimental Botany 73, 1104–1121. ecology—taking biomechanics to the field) meetings, certainly Kwok R. 2017. Field instruments: build it yourself. Nature 545, 253–255. attests to the timeliness of the topic. Langer M, Hegge E, Speck T, Speck O. 2022. Acclimations to wind loads and/or contact stimuli? A biomechanical study of peltate leaves of Pilea peperomioides. Journal of Experimental Botany 72, 1236–1252. Funding Lauderbagh LK, Holder CD. 2022. The biomechanics of leaf oscillations during rainfall events. Journal of Experimental Botany 73, 1139–1154. UB is funded by a Royal Society University Research Fellowship Lenz A-K, Bauer U, Ruxton GD. 2022. An ecological perspective on water (UF150138). shedding from leaves. Journal of Experimental Botany 73, 1176–1189. Middendorf BJ, Prasad PVV, Pierzynski GM. 2020. Setting research Keywords: Climate change, ecomechanics, field work, functional priorities for tackling climate change. Journal of Experimental Botany 71, morphology, interdisciplinary, mechanical ecology, mechanical stress. 480–489.
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