New insights and opportunities from taking a biomechanical perspective on plant ecology - Oxford Academic

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New insights and opportunities from taking a biomechanical perspective on plant ecology - Oxford Academic
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

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This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/),
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New insights and opportunities from taking a biomechanical perspective on plant ecology - Oxford Academic
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
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