How kelp in drag lose their ruffles: environmental cues, growth kinematics, and mechanical constraints govern curvature

We reveal how patterns of growth in response to environmental cues can produce curvature in biological structures by setting up mechanical stresses that cause elastic buckling. Nereocystis luetkeana are nearshore kelp with wide ruffled blades that minimize self-shading in slow flow, but narrow flat...

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Published in:Journal of experimental botany Vol. 72; no. 10; pp. 3677 - 3687
Main Authors: Koehl, Mimi A R, Silk, Wendy K
Format: Journal Article
Language:English
Published: England 04-05-2021
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Abstract We reveal how patterns of growth in response to environmental cues can produce curvature in biological structures by setting up mechanical stresses that cause elastic buckling. Nereocystis luetkeana are nearshore kelp with wide ruffled blades that minimize self-shading in slow flow, but narrow flat blades that reduce hydrodynamic drag in rapid flow. Previously we showed that blade ruffling is a plastic trait associated with a transverse gradient in longitudinal growth. Here we consider expansion and displacement of tissue elements due to growth in blades, and find that growth patterns are altered by tensile stress due to hydrodynamic drag, but not by shading or nutrients. When longitudinal stress in a blade is low in slow flow, blade edges grow faster than the midline in young tissue near the blade base. Tissue elements are displaced distally by expansion of younger proximal tissue. Strain energy caused by the transverse gradient in longitudinal growth is released by elastic buckling once the blade grows wide enough, producing ruffles distal to the region where the growth inhomogeneity started. If a blade experiences higher stress in rapid flow, the edges and midline grow at the same rate, so the blade becomes flat as these new tissue elements are displaced distally.
AbstractList We reveal how patterns of growth in response to environmental cues can produce curvature in biological structures by setting up mechanical stresses that cause elastic buckling. Nereocystis luetkeana are nearshore kelp with wide ruffled blades that minimize self-shading in slow flow, but narrow flat blades that reduce hydrodynamic drag in rapid flow. Previously we showed that blade ruffling is a plastic trait associated with a transverse gradient in longitudinal growth. Here we consider expansion and displacement of tissue elements due to growth in blades, and find that growth patterns are altered by tensile stress due to hydrodynamic drag, but not by shading or nutrients. When longitudinal stress in a blade is low in slow flow, blade edges grow faster than the midline in young tissue near the blade base. Tissue elements are displaced distally by expansion of younger proximal tissue. Strain energy caused by the transverse gradient in longitudinal growth is released by elastic buckling once the blade grows wide enough, producing ruffles distal to the region where the growth inhomogeneity started. If a blade experiences higher stress in rapid flow, the edges and midline grow at the same rate, so the blade becomes flat as these new tissue elements are displaced distally.
Author Silk, Wendy K
Koehl, Mimi A R
Author_xml – sequence: 1
  givenname: Mimi A R
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  surname: Silk
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  organization: Department of Land, Air, and Water Resources, University of California, Davis, CA, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33718962$$D View this record in MEDLINE/PubMed
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Issue 10
Keywords stress adaptation
Buckling of thin plates
environmental plasticity
morphogenesis
kelp
growth kinematics
Language English
License The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.
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Snippet We reveal how patterns of growth in response to environmental cues can produce curvature in biological structures by setting up mechanical stresses that cause...
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SubjectTerms Biomechanical Phenomena
Cues
Kelp
Phaeophyceae
Title How kelp in drag lose their ruffles: environmental cues, growth kinematics, and mechanical constraints govern curvature
URI https://www.ncbi.nlm.nih.gov/pubmed/33718962
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