Bivalves rapidly repair shells damaged by fatigue and bolster strength

Abstract

Hard external armors have to defend against a lifetime of threats yet are traditionally understood by their ability to withstand a single attack. Survival of bivalve mollusks thus can depend on the ability to repair shell damage between encounters. We studied the capacity for repair in the intertidal mussel Mytilus californianus by compressing live mussels for 15 cycles at ∼79% of their predicted strength (critically fracturing 46% of shells), then allowing the survivors 0, 1, 2 or 4 weeks to repair. Immediately after fatigue loading, mussel shells were 20% weaker than control shells that had not experienced repetitive loading. However, mussels restored full shell strength within 1 week, and after 4 weeks shells that had experienced greater fatiguing forces were stronger than those repetitively loaded at lower forces. Microscopy supported the hypothesis that crack propagation is a mechanism of fatigue-caused weakening. However, the mechanism of repair was only partially explained, as epifluorescence microscopy of calcein staining for shell deposition showed that only half of the mussels that experienced repetitive loading had initiated direct repair via shell growth around fractures. Our findings document repair weeks to months faster than demonstrated in other mollusks. This rapid repair may be important for the mussels’ success contending with predatory and environmental threats in the harsh environment of wave-swept rocky coasts, allowing them to address non-critical but weakening damage and to initiate plastic changes to shell strength. We highlight the significant insight gained by studying biological armors not as static structures but, instead, as dynamic systems that accumulate, repair and respond to damage.

Long-Term Monitoring of Rocky Intertidal Communities: Lessons and Implications from the Redwood National and State Parks, Northern California

“…Why they were less common in the Fucus and Mytilus plots is unknown. For mussels, perhaps the protection offered by their shells (e.g., Burnett and Belk 2018, Crane et al 2021), along with their ability to increase attachment strength in response to increased hydrodynamic forces (e.g., Witman and Suchanek 1984, Bell and Gosline 1997, Carrington 2002), offer them heightened levels of protection from some disturbances. For F. gardneri, because it is a canopy-forming species, the measures of its abundance reflect the size of the canopy, not the space it occupies on the rock.…”

Mussels Repair Shell Damage despite Limitations Imposed by Ocean Acidification

“…In studies of gastropods that employed flat plate compression testing, mechanical stress produced cracks that propagated along growth lines rather than repaired shell, resulting in no impact on shell integrity [36,93]. Similarly, M. californianus has been found to repair shell fatigue damage, with repaired shell often exceeding the strength of unrepaired shell after 4 weeks [37]. However, these results are not comparable as the mechanical testing employed in this study was designed to estimate the effort required of a secondary predator to reach the mantle cavity through the repaired material.…”

“…To mitigate these risks, mussels and other mollusk species are capable of quickly repairing a shell injury by patching holes [30][31][32]. Using this strategy, mollusks seal off the mantle cavity within hours or days [33,34], although weeks or months may be required to regain the structural integrity of unrepaired shell [35][36][37].…”