To bend a coralline: effect of joint morphology on flexibility and stress amplification in an articulated calcified seaweed

King

2016

Self Cite

Flexibility is key to survival for seaweeds exposed to the extreme hydrodynamic environment of wave-washed rocky shores. This poses a problem for coralline algae, whose calcified cell walls make them rigid. Through the course of evolution, erect coralline algae have solved this problem by incorporating joints (genicula) into their morphology, allowing their fronds to be as flexible as those of uncalcified seaweeds. To provide the flexibility required by this structural innovation, the joint material of Calliarthron cheilosporioides, a representative articulated coralline alga, relies on an extraordinary tissue that is stronger, more extensible and more fatigue resistant than the tissue of other algal fronds. Here, we report on experiments that reveal the viscoelastic properties of this material. On the one hand, its compliance is independent of the rate of deformation across a wide range of deformation rates, a characteristic of elastic solids. This deformation rate independence allows joints to maintain their flexibility when loaded by the unpredictable -and often rapidly imposed -hydrodynamic force of breaking waves. On the other hand, the genicular material has viscous characteristics that similarly augment its function. The genicular material dissipates much of the energy absorbed as a joint is deformed during cyclic wave loading, which potentially reduces the chance of failure by fatigue, and the material accrues a limited amount of deformation through time. This limited creep increases the flexibility of the joints while preventing them from gradually stretching to the point of failure. These new findings provide the basis for understanding how the microscale architecture of genicular cell walls results in the adaptive mechanical properties of coralline algal joints.

Section: Discussionsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

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The extraordinary joint material of an articulated coralline alga. I. Mechanical characterization of a key adaptation

King

2016

Self Cite

“…However, some coralline algae -the erect, articulated corallines -have avoided this limitation through the evolution of joints (genicula) that allow their fronds to be as flexible as those of other seaweeds. The flexibility provided by these joints depends on the unusual mechanical properties of the genicular tissue (Martone and Denny, 2008;Janot and Martone, 2016), and these properties are best understood for Calliarthron cheilosporioides Manza, a representative articulated coralline found on the West Coast of North America.…”

Section: Introductionmentioning

confidence: 99%

The extraordinary joint material of an articulated coralline alga. II. Modeling the structural basis of its mechanical properties

King

2016

Self Cite

By incorporating joints into their otherwise rigid fronds, erect coralline algae have evolved to be as flexible as other seaweeds, which allows them to thrive -and even dominate space -on wave-washed shores around the globe. However, to provide the required flexibility, the joint tissue of Calliarthron cheilosporioides, a representative articulated coralline alga, relies on an extraordinary tissue that is stronger, more extensible and more fatigue resistant than that of other algae. Here, we used the results from recent experiments to parameterize a conceptual model that links the microscale architecture of cell walls to the adaptive mechanical properties of joint tissue. Our analysis suggests that the theory of discontinuous fiber-wound composite materials (with cellulose fibrils as the fibers and galactan gel as the matrix) can explain key aspects of the material's mechanics. In particular, its adaptive viscoelastic behavior can be characterized by two, widely separated time constants. We speculate that the short time constant (∼14 s) results from the viscous response of the matrix to the change in cell-wall shape as a joint is stretched, a response that allows the material both to remain flexible and to dissipate energy as a frond is lashed by waves. We propose that the long time constant (∼35 h), is governed by the shearing of the matrix between cellulose fibrils. The resulting high apparent viscosity ensures that joints avoid accumulating lethal deformation in the course of a frond's lifetime. Our synthesis of experimental measurements allows us to draw a chain of mechanistic inference from molecules to cell walls to fronds and community ecology.

“…In order for the frond (technically, the thallus) of a coralline alga to have the same flexibility as that of non-calcified algae, the genicula (which comprise only ~15% of branch length) (Martone and Denny, 2008a) must be more flexible than the tissues of fleshy seaweeds. This increased flexibility is achieved through a combination of morphology and material properties (Martone, 2006;Martone and Denny, 2008a).…”

Section: Introductionmentioning

confidence: 99%

Indefatigable: an erect coralline alga is highly resistant to fatigue

Mach

Tepler

et al. 2013

SUMMARYIntertidal organisms are subjected to intense hydrodynamic forces as waves break on the shore. These repeated insults can cause a plant or animal's structural materials to fatigue and fail, even though no single force would be sufficient to break the organism. Indeed, the survivorship and maximum size of at least one species of seaweed is set by the accumulated effects of small forces rather than the catastrophic imposition of a single lethal force. One might suppose that fatigue would be especially potent in articulated coralline algae, in which the strain of the entire structure is concentrated in localized joints, the genicula. However, previous studies of joint morphology suggest an alternative hypothesis. Each geniculum is composed of a single tier of cells, which are attached at their ends to the calcified segments of the plant (the intergenicula) but have minimal connection to each other along their lengths. This lack of neighborly attachment potentially allows the weak interfaces between cells to act as 'crack stoppers', inhibiting the growth of fatigue cracks. We tested this possibility by repeatedly loading fronds of Calliarthron cheilosporioides, a coralline alga common on wave-washed shores in California. When repeatedly loaded to 50-80% of its breaking strength, C. cheilosporioides commonly survives more than a million stress cycles, with a record of 51 million. We show how this extraordinary fatigue resistance interacts with the distribution of wave-induced water velocities to set the limits to size in this species.