How kelp produce blade shapes suited to different flow regimes: A new wrinkle.

Many species of macroalgae have flat, strap-like blades in habitats exposed to rapidly flowing water, but have wide, ruffled "undulate" blades at protected sites. We used the giant bull kelp, Nereocystis luetkeana, to investigate how these ecomorphological differences are produced. The undulate blades of N. luetkeana from sites with low flow remain spread out and flutter erratically in moving water, thereby not only enhancing interception of light, but also increasing drag. In contrast, strap-like blades of kelp from habitats with rapid flow collapse into streamlined bundles and flutter at low amplitude in flowing water, thus reducing both drag and interception of light. Transplant experiments in the field revealed that shape of the blade in N. luetkeana is a plastic trait. Laboratory experiments in which growing blades from different sites were subjected to tensile forces that mimicked the hydrodynamic drag experienced by blades in different flow regimes showed that change in shape is induced by mechanical stress. During growth experiments in the field and laboratory, we mapped the spatial distribution of growth in both undulate and strap-like blades to determine how these different morphologies were produced. The highest growth rates occur near the proximal ends of N. luetkeana blades of both morphologies, but the rates of transverse growth of narrow, strap-like blades are lower than those of wide, undulate blades. If rates of longitudinal growth at the edges of a blade exceed the rate of longitudinal growth along the midline of the blade, ruffles along the edges of the blade are produced by elastic buckling. In contrast, flat blades are produced when rates of longitudinal growth are similar across the width of a blade. Because ruffles are the result of elastic buckling, a compliant undulate N. luetkeana blade can easily be pushed into different configurations (e.g., the wavelengths of the ruffles along the edges of the blade can change, and the whole blade can twist into left- and right-handed helicoidal shapes), which may enhance movements of the blade in flowing water that reduce self-shading and increase mass exchange along blade surfaces.

[1]  Jürgen Jost,et al.  Geometry and Physics , 2009 .

[2]  R. Scheibling,et al.  Effect of wave exposure on morphology, attachment strength and survival of the invasive green alga Codium fragile ssp. tomentosoides , 2007 .

[3]  P. Martone Kelp versus coralline: cellular basis for mechanical strength in the wave‐swept seaweed Calliarthron (Corallinaceae, Rhodophyta) 1 , 2007 .

[4]  J. Leichter,et al.  Topographic shading and wave exposure influence morphology and ecophysiology of Ecklonia radiata (C. Agardh 1817) in Fiordland, New Zealand , 2007 .

[5]  Johanna H. Rosman,et al.  Spatial patterns of flow and their modification within and around a giant kelp forest , 2007 .

[6]  M. Boller,et al.  Interspecific comparison of hydrodynamic performance and structural properties among intertidal macroalgae , 2007, Journal of Experimental Biology.

[7]  Bryce D. Wolcott Mechanical size limitation and life-history strategy of an intertidal seaweed , 2007 .

[8]  Eran Sharon,et al.  Geometrically driven wrinkling observed in free plastic sheets and leaves. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[9]  Ralph T. Clarke,et al.  The drag and reconfiguration experienced by five macrophytes from a lowland river. , 2007 .

[10]  R. Carpenter,et al.  Habitat-induced morphological variation influences photosynthesis and drag on the marine macroalga Pachydictyon coriaceum , 2007 .

[11]  Johanna H. Rosman,et al.  A field investigation into the effects of a kelp forest (Macrocystis pyrifera) on coastal hydrodynamics and transport , 2007 .

[12]  J. Dumais Can mechanics control pattern formation in plants? , 2007, Current opinion in plant biology.

[13]  Bruno Moulia,et al.  A frequency lock-in mechanism in the interaction between wind and crop canopies , 2006, Journal of Fluid Mechanics.

[14]  M. Boller,et al.  In situ measurements of hydrodynamic forces imposed on Chondrus crispus Stackhouse , 2006 .

[15]  P. Schopfer,et al.  Biomechanics of plant growth. , 2006, American journal of botany.

[16]  Mark W. Denny Ocean waves, nearshore ecology, and natural selection , 2006, Aquatic Ecology.

[17]  Emily Carrington,et al.  The hydrodynamic effects of shape and size change during reconfiguration of a flexible macroalga , 2006, Journal of Experimental Biology.

[18]  P. Martone Size, strength and allometry of joints in the articulated coralline Calliarthron , 2006, Journal of Experimental Biology.

[19]  M. Sheetz,et al.  Local force and geometry sensing regulate cell functions , 2006, Nature Reviews Molecular Cell Biology.

[20]  H. Stewart Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef , 2006 .

[21]  T. Wernberg,et al.  Differences in kelp morphology between wave sheltered and exposed localities: morphologically plastic or fixed traits? , 2006 .

[22]  H. Stewart ONTOGENETIC CHANGES IN BUOYANCY, BREAKING STRENGTH, EXTENSIBILITY, AND REPRODUCTIVE INVESTMENT IN A DRIFTING MACROALGA TURBINARIA ORNATA (PHAEOPHYTA) 1 , 2006 .

[23]  Bela H. Buck,et al.  Response of offshore cultivated Laminaria saccharina to hydrodynamic forcing in the North Sea , 2005 .

[24]  D. Cosgrove Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[25]  T. Baskin Anisotropic expansion of the plant cell wall. , 2005, Annual review of cell and developmental biology.

[26]  T. Wernberg,et al.  The effect of wave exposure on the morphology of Ecklonia radiata , 2005 .

[27]  J. Kitzes,et al.  Red Algae Respond to Waves: Morphological and Mechanical Variation in Mastocarpus papillatus Along a Gradient of Force , 2005, The Biological Bulletin.

[28]  Thomas Speck,et al.  Reconfiguration as a Prerequisite for Survival in Highly Unstable Flow-Dominated Habitats , 2004, Journal of Plant Growth Regulation.

[29]  Janet Braam,et al.  In touch: plant responses to mechanical stimuli. , 2004, The New phytologist.

[30]  Loretta M. Roberson,et al.  Variation in blade morphology of the kelp Eisenia arborea: incipient speciation due to local water motion? , 2004 .

[31]  J. Braam,et al.  Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. , 2004, The New phytologist.

[32]  G. Schoch,et al.  The Role of Estuarine Hydrodynamics in the Distribution of Kelp Forests in Kachemak Bay, Alaska** , 2004 .

[33]  H. Stewart Hydrodynamic consequences of maintaining an upright posture by different magnitudes of stiffness and , 2004 .

[34]  Natasha K Li,et al.  Limits to Phenotypic Plasticity: Flow Effects on Barnacle Feeding Appendages , 2004, The Biological Bulletin.

[35]  K. Milligan,et al.  Morphological variations do not effectively reduce drag forces at high wave-exposure for the macroalgal species, Hedophyllum sessile (Laminariales, Phaeophyta) , 2004 .

[36]  R. Gordon,et al.  Effects of water motion on propagule release from algae with complex life histories , 2004 .

[37]  T. Klinger,et al.  Population, morphometric and biomechanical studies of three understory kelps along a hydrodynamic gradient , 2003 .

[38]  R. Carpenter,et al.  THE EFFECTS OF MORPHOLOGY AND WATER FLOW ON PHOTOSYNTHESIS OF MARINE MACROALGAE , 2003 .

[39]  E. Coen,et al.  Genetic Control of Surface Curvature , 2003, Science.

[40]  L. Mahadevan,et al.  Geometry and physics of wrinkling. , 2003, Physical review letters.

[41]  H. Swinney,et al.  Buckling cascades in free sheets , 2002 .

[42]  S. Gaines,et al.  Geographic variability in form, size and survival of Egregia menziesii around Point Conception, California , 2002 .

[43]  R. Staples,et al.  Thigmo responses in plants and fungi. , 2002, American journal of botany.

[44]  Terrie Klinger,et al.  Interactive roles of mesograzers and current flow in survival of kelps , 2001 .

[45]  S. Kawamata Adaptive mechanical tolerance and dislodgement velocity of the kelp Laminaria japonica in wave-induced water motion , 2001 .

[46]  B. Moulia,et al.  Biomechanical study of the effect of a controlled bending on tomato stem elongation: global mechanical analysis. , 2000, Journal of experimental botany.

[47]  J. Shaffer Seasonal Variation in Understory Kelp Bed Habitats of the Strait of Juan de Fuca , 2000 .

[48]  C. Hurd,et al.  WATER MOTION, MARINE MACROALGAL PHYSIOLOGY, AND PRODUCTION , 2000, Journal of phycology.

[49]  M. Koehl,et al.  Ecological biomechanics of benthic organisms: life history, mechanical design and temporal patterns of mechanical stress. , 1999, The Journal of experimental biology.

[50]  A. Trewavas How plants learn. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[51]  E. Serrão,et al.  CONTROL OF GAMETE RELEASE IN FUCOID ALGAE: SENSING HYDRODYNAMIC CONDITIONS VIA CARBON ACQUISITION , 1998 .

[52]  Denny,et al.  Flow and flexibility. II. The roles of size and shape in determining wave forces on the bull kelp nereocystis luetkeana , 1997, The Journal of experimental biology.

[53]  G. Jackson Currents in the high drag environment of a coastal kelp stand off California , 1997 .

[54]  C. Blanchette SIZE AND SURVIVAL OF INTERTIDAL PLANTS IN RESPONSE TO WAVE ACTION: A CASE STUDY WITH FUCUS GARDNERI , 1997 .

[55]  C. Hurd,et al.  FLOW VISUALIZATION AROUND SINGLE‐ AND MULTIPLE‐BLADED SEAWEEDS WITH VARIOUS MORPHOLOGIES 1 , 1997 .

[56]  C. Hurd,et al.  Visualization of seawater flow around morphologically distinct forms of the giant kelp Macrocystis integrifolia from wave‐sheltered and exposed sites , 1997 .

[57]  Janet E. Kübler,et al.  Temperature dependent change in the complexity of form of Chondrus crispus fronds , 1996 .

[58]  C. Hurd,et al.  Effect of seawater velocity on inorganic nitrogen uptake by morphologically distinct forms of Macrocystis integrifolia from wave-sheltered and exposed sites , 1996 .

[59]  F. Shaughnessy,et al.  Consequences of morphology and tissue strength to blade survivorship of two closely related Rhodophyta species , 1996 .

[60]  P. B. Green,et al.  Phyllotactic Patterns: A Biophysical Mechanism for their Origin , 1996 .

[61]  Robert A. Smith,et al.  EFFECT OF CURRENT VELOCITY ON THE DETACHMENT OF THALLI OF ULVA LACTUCA (CHLOROPHYTA) IN A NEW ZEALAND ESTUARY , 1995 .

[62]  S. Fredriksen,et al.  Growth allocation in Laminaria hyperborea (Laminariales, Phaeophyceae) in relation to age and wave exposure , 1995 .

[63]  W. C. O'Reilly,et al.  Effects of Southern California Kelp Beds on Waves , 1995 .

[64]  Johnson,et al.  MAINTENANCE OF DYNAMIC STRAIN SIMILARITY AND ENVIRONMENTAL STRESS FACTOR IN DIFFERENT FLOW HABITATS: THALLUS ALLOMETRY AND MATERIAL PROPERTIES OF A GIANT KELP , 1994, The Journal of experimental biology.

[65]  R. Atalla,et al.  Influence of hydrodynamic environment on composition and macromolecular organization of structural polysaccharides in Egregia menziesii cell walls , 1994, Planta.

[66]  S. Dudgeon,et al.  Thick vs. thin: thallus morphology and tissue mechanics influence differential drag and dislodgement of two co-dominant seaweeds , 1992 .

[67]  P. Green Pattern Formation in Shoots: A Likely Role for Minimal Energy Configurations of the Tunica , 1992, International Journal of Plant Sciences.

[68]  M. Littler,et al.  Marine Algae of California , 1992 .

[69]  C. Fernández,et al.  WATER MOTION AND MORPHOLOGY IN CHONDRUS CRISPUS (RHODOPHYTA) 1 , 1992 .

[70]  G. Kraemer,et al.  Effects of tensile force and nutrient availability on carbon uptake and cell wall synthesis in blades of juvenile Egregia menziesii (Turn.) Aresch. (Phaeophyta) , 1991 .

[71]  G. Kraemer,et al.  BIOMECHANICS AND ALGINIC ACID COMPOSITION DURING HYDRODYNAMIC ADAPTATION BY EGREGIA MENZIESII (PHAEOPHYTA) JUVENILES 1 , 1991 .

[72]  K. Mann,et al.  Herbivore-like damage induces increased strength and toughness in a seaweed , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[73]  J. Bolton,et al.  Form variation and productivity of an intertidal foliose Gigartina species (Rhodophyta) in relation to wave exposure , 1990, Hydrobiologia.

[74]  E. Carrington Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing , 1990 .

[75]  S. L. Armstrong The behavior in flow of the morphologically variable seaweed Hedophyllum sessile (C. Ag.) Setchell , 1989, Hydrobiologia.

[76]  Randall S. Alberte,et al.  Flow, flapping, and photosynthesis ofNereocystis leutkeana: a functional comparison of undulate and flat blade morphologies , 1988 .

[77]  Thomas J. Givnish,et al.  On the economy of plant form and function. , 1988 .

[78]  Nelson,et al.  Defects in flexible membranes with crystalline order. , 1988, Physical review. A, General physics.

[79]  V. A. Gerard Hydrodynamic streamlining of Laminaria saccharina Lamour. in response to mechanical stress , 1987 .

[80]  S. Palumbi,et al.  Tactics of Acclimation: Morphological Changes of Sponges in an Unpredictable Environment , 1984, Science.

[81]  Steven Vogel,et al.  Drag and Flexibility in Sessile Organisms , 1984 .

[82]  M. J. Wynne,et al.  The Biology of seaweeds , 1982 .

[83]  L. Druehl,et al.  Morphological and growth responses of geographically isolated Macrocystis integrifolia populations when grown in a common environment , 1982 .

[84]  E. J. Paula,et al.  Wave exposure and ecotypical differentiation in Sargassum cymosum (Phaeophyta—Fucales) , 1982 .

[85]  M. Littler,et al.  The Evolution of Thallus Form and Survival Strategies in Benthic Marine Macroalgae: Field and Laboratory Tests of a Functional Form Model , 1980, The American Naturalist.

[86]  K. Mann,et al.  GROWTH AND PRODUCTION OF LAMINARIA LONGICRURIS (PHAEOPHYTA) POPULATIONS EXPOSED TO DIFFERENT INTENSITIES OF WATER MOVEMENT 1 , 1979 .

[87]  S. A. Wainwright,et al.  Mechanical adaptations of a giant kelp , 1977 .

[88]  M. A. R. Koehl,et al.  Effects of Sea Anemones on the Flow Forces They Encounter , 1977 .

[89]  R. Black The Effects of Grazing by the Limpet, Acmaea Insessa, on the Kelp, Egregia Laevigata, in the Intertidal Zone , 1976 .

[90]  A. Chapman The genetic basis of morphological differentiation in some Laminaria populations , 1974 .

[91]  P. Svendsen,et al.  The taxonomic status, distribution, and morphology of Laminaria cucullata Sensu Jorde and Klavestad , 1971 .

[92]  T. Norton Growth form and environment in Saccorhiza polyschides , 1969, Journal of the Marine Biological Association of the United Kingdom.

[93]  R. O. Erickson,et al.  Relative Elemental Rates and Anisotropy of Growth in Area: a Computer Programme , 1966 .

[94]  M. Parke Studies on British Laminariaceae. I. Growth in Laminaria Saccharina (L.) Lamour , 1948, Journal of the Marine Biological Association of the United Kingdom.

[95]  G. M. Smith THE MARINE ALGAE OF CALIFORNIA. , 1945, Science.

[96]  W. R. Dean On the Theory of Elastic Stability , 1925 .

[97]  M. Kikuyama,et al.  Mechanosensitive Ion Channels in Chara: Influence of Water Channel Inhibitors, HgCl2 and ZnCl2, on Generation of Receptor Potential , 2007, Journal of Membrane Biology.

[98]  G. Kendrick,et al.  The effect of thallus size, life stage, aggregation, wave exposure and substratum conditions on the forces required to break or dislodge the small kelp Ecklonia radiata , 2004 .

[99]  Michael P Marder,et al.  Leaves, flowers and garbage bags: Making waves , 2004 .

[100]  J. Bolton,et al.  The Effects of Wave Exposure and Depth on the Morphology of Inshore Populations of the Namibian Kelp, Laminaria schinzii Foslie , 1996 .

[101]  S. Bäck Morphological variation of northern Baltic Fucus vesiculosus along the exposure gradient , 1993 .

[102]  R. de Nys,et al.  The Cytokinins as Endogenous Growth Regulators in Macrocystis pyrifera (L.) C. Ag. (Phaeophyceae) , 1990 .

[103]  N. Hallam,et al.  Morphological Differences in the Southern Bull-Kelp (Durvillaea potatorum) throughout South-Eastern Australia , 1989 .

[104]  C. Brooks Computer simulation of liquids , 1989 .

[105]  M. Haynes Morphology and environment. , 1988 .

[106]  T. Norton The ecology of macroalgae in the Firth of Clyde , 1986 .

[107]  W. Silk,et al.  Quantitative Descriptions of Development , 1984 .

[108]  T. Norton,et al.  A Review of Some Aspects of Form and Function in Seaweeds , 1982 .

[109]  F. I. Dromgoole Form and Function of the Pneumatocysts of Marine Algae. II. Variations in Morphology and Resistance to Hydrostatic Pressure , 1981 .

[110]  M. Koehl,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Modulation of wave forces on kelp canopies by alongshore currents , 2022 .