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

Abstract

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.

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

“…From the high strain rate experiments conducted in the companion paper (Denny and King, 2016), we estimate that E 2 (at ε=0.2, a strain typical of our cyclical stress-strain experiments) is approximately 27 MPa. From the average creep of genicula in tension (Denny and King, 2016), we estimate (using Eqn 5) that μ 2 is approximately 5×10 12 Pa s, and from stress relaxation tests (Denny and King, 2016), we estimate that μ 1 is approximately 3.9×10 8 Pa s. Through trial and error, we then estimate that E 1 is 40 MPa.…”

“…These relationships allow us to estimate E 2 and μ 2 in our model using data from experiments regarding stiffness and creep reported in the companion paper (Denny and King, 2016). When the entire model is strained at a sufficiently high rate, both dashpots are 'frozen' and the model's stiffness is due to spring 2 alone.…”

“…1B). Neither breaking stress nor the material's compliance (strain per stress) is significantly correlated with the rate of strain, again typical of an elastic solid (Denny and King, 2016). By contrast, other aspects of the tissue's mechanical behavior reveal viscous tendencies.…”

“…Furthermore, the tissue exhibits an unusual combination of elastic and viscous properties (Denny and King, 2016). As one would expect from an elastic solid, the stress (force per cross-sectional area) required to extend the material increases in proportion to strain (the change in length per unstressed length) (Fig.…”

“…Together, these material properties allow genicula to provide the flexibility C. cheilosporioides' fronds need to survive -and even dominate space -in the surf zone, while resisting fracture from fatigue and lethal strain from creep (Denny and King, 2016). Indeed, C. cheilosporioides can act as an ecosystem engineer: its densely packed fronds serve as a shelter for invertebrate animals.…”