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 |
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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. |
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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 orcidid: 0000-0002-0633-1623 surname: Koehl fullname: Koehl, Mimi A R organization: Department of Integrative Biology, University of California, Berkeley, CA, USA – sequence: 2 givenname: Wendy K orcidid: 0000-0002-2202-2505 surname: Silk fullname: Silk, Wendy K 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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CitedBy_id | crossref_primary_10_1093_jxb_erab498 crossref_primary_10_1111_jpy_13408 crossref_primary_10_1093_jxb_erab536 crossref_primary_10_1007_s10499_024_01422_6 crossref_primary_10_1146_annurev_marine_032223_014227 crossref_primary_10_1242_jeb_245442 crossref_primary_10_1007_s10811_023_03061_5 |
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ContentType | Journal Article |
Copyright | 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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Keywords | stress adaptation Buckling of thin plates environmental plasticity morphogenesis kelp growth kinematics |
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Title | How kelp in drag lose their ruffles: environmental cues, growth kinematics, and mechanical constraints govern curvature |
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