Mechanical and biological consequences of repetitive loading: crack initiation and fatigue failure in the red macroalga Mazzaella

Abstract

SUMMARYOn rocky shores, wave-swept macroalgae experience dramatic and repeated wave-induced hydrodynamic forces. However, previous studies of macroalgal mechanics have shown that individual waves are not forceful enough to account for observed rates of breakage. Instead, fatigue may contribute to algal breakage, with damage accumulating over time in conditions of repeated loading. Here I examine the entire process of fatigue, from crack initiation to eventual specimen fracture, in the common red alga Mazzaella. Propensity for fatigue failure in laboratory tests varied with life history phase and species: at a given repeated loading stress, male gametophytes endured more loading cycles before breakage than tetrasporophytes, which in turn lasted longer than female gametophytes; likewise, M. splendens withstood more loading cycles at a given repeated loading stress than M. flaccida. Fatigue failure begins with formation of cracks, the timing and location of which were assessed. Cracks formed, on average, after approximately 80-90% of cycles required for failure had passed, although crack timing varied with life history phase. Also, crack formation frequently occurred in association with endophytes and female gametophyte reproductive structures, suggesting a cost of endophyte infection and a tradeoff between reproduction and mechanical survival. Comparison between laboratory and field loading conditions provides robust confirmation that fatigue breaks fronds in natural M. flaccida populations. Large, female gametophyte fronds are predicted to be most susceptible to fatigue failure in the field, whereas small, male gametophyte fronds are least likely to break.

Failure by fatigue in the field: a model of fatigue breakage for the macroalga Mazzaella, with validation

“…Fatigue behavior of M. flaccida has been quantified previously with standard laboratory measurement techniques (Mach, 2009). In the approach employed, each blade specimen was extended to a given tensile force and then relaxed to 0N, repeatedly, until the specimen broke.…”

“…Hansen and Doyle, 1976;Foster, 1982;Seymour et al, 1989;Dudgeon and Johnson,eventually cause specimen fracture. Mach (Mach, 2009) then documented that the entire process of fatigue failure, from the formation of small cracks through their growth to the point of specimen rupture, occurs predictably in the seaweed Mazzaella. It has thus been established that flat-bladed seaweeds fail by fatigue in standard laboratory loading conditions.…”

“…The traditional approach has involved determination of a seaweed's breaking strength and comparison of this strength with maximal wave-induced force, with breakage often under-predicted (Koehl and Alberte, 1988;Gaylord et al, 1994;Johnson and Koehl, 1994;Friedland and Denny, 1995;Utter and Denny, 1996;Denny et al, 1997;Johnson, 2001;Kitzes and Denny, 2005). Researchers have suggested that other factors, such as damage due to herbivory, abrasion or physiological stressors, may account for observed breakage rates, weakening fronds that individual waves then break (Friedland and Denny, 1995;Utter and Denny, 1996;Kitzes and Denny, 2005;Denny, 2006).Additionally, researchers have investigated the possibility that seaweeds break not just from large individual wave-imposed forces but from damage accumulated over a series of wave-imposed forces (Hale, 2001;Mach et al, 2007a;Mach et al, 2007b;Mach, 2009 Accepted 24 January 2011 SUMMARY Seaweeds inhabiting the extreme hydrodynamic environment of wave-swept shores break frequently. However, traditional biomechanical analyses, evaluating breakage due to the largest individual waves, have perennially underestimated rates of macroalgal breakage.…”

“…Additionally, researchers have investigated the possibility that seaweeds break not just from large individual wave-imposed forces but from damage accumulated over a series of wave-imposed forces (Hale, 2001;Mach et al, 2007a;Mach et al, 2007b;Mach, 2009 Accepted 24 January 2011 SUMMARY Seaweeds inhabiting the extreme hydrodynamic environment of wave-swept shores break frequently. However, traditional biomechanical analyses, evaluating breakage due to the largest individual waves, have perennially underestimated rates of macroalgal breakage.…”

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

“…Because joints do not weaken appreciably through repeated loadings, whether a frond will survive or not is determined by the largest force it encounters. (This is in contrast to fleshy red algae, in which the accumulated damage from small forces limits size; Mach, 2009;Mach et al, 2007Mach et al, , 2011 Thus, from easily acquired records of maximum wave force (Denny and Wethey, 2001), one can accurately estimate the maximum size to which C. cheilosporioides' fronds can grow in a given wave environment (Martone and Denny, 2008a;Denny, 2016). Because C. cheilosporioides is a major competitor for space in the low intertidal zone, these estimates of maximum size can be valuable when considering the ecological consequences of a changing wave climate.…”