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

Journal of Experimental Biology

Volumn 212, Issue 7, 2009, Pages 961-976

  Mach, Katharine J ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Biomechanics; Breakage; Crack growth; Crack initiation; Endophytes; Fatigue; Life history phases; Macroalgae; Mazzaella; Seaweed

Indexed keywords

ANALYSIS OF VARIANCE; ARTICLE; BIOMECHANICS; BIOPHYSICS; ENVIRONMENT; MECHANICAL STRESS; PHYSIOLOGY; RED ALGA; SEASON; SPECIES DIFFERENCE; TENSILE STRENGTH; TIME; UNITED STATES;

ALGAE, RED; ANALYSIS OF VARIANCE; BIOMECHANICS; BIOPHYSICS; CALIFORNIA; ENVIRONMENT; SEASONS; SPECIES SPECIFICITY; STRESS, MECHANICAL; TENSILE STRENGTH; TIME FACTORS;

ALGAE; MAZZAELLA; MAZZAELLA FLACCIDA; MAZZAELLA SPLENDENS; RHODOPHYTA;

EID: 63849175324     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.026989     Document Type: Article

References (105)

1. Abbot, I. A. and Hollenberg, G. J. (1976). Marine Algae of California. Stanford, CA: Stanford University Press.
2. Apt, K. E. (1984). Effects of the symbiotic red alga Hypneocolax stellaris on its host Hypnea musciformis (Hypneaceae, Gigartinales). J. Phycol. 20, 148-150.
3. Arampatzis, A., Karamanidis, K. and Albracht, K. (2007). Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. J. Exp. Biol. 210, 2743-2753.
4. Armstrong, S. L. (1987). Mechanical properties of the tissues of the brown alga Hedophyllum sessile (C. Ag.) Setchell: variability with habitat. J. Exp. Mar. Biol. Ecol. 114, 143-151.
5. Baskerville, G. L. (1972). Use of logarithmic regression in the estimation of plant biomass. Can. J. For. Res. 2, 49-53.
6. Beauchamp, J. J. and Olson, J. S. (1973). Corrections for bias in regression estimates after logarithmic transformation. Ecology 54, 1403-1407.
7. Bell, G. (1984a). Measuring the cost of reproduction. I. The correlation structure of the life table of a plankton rotifer. Evolution 38, 300-313.
8. Bell, G. (1984b). Measuring the cost of reproduction. II. The correlation structure of the life tables of five freshwater invertebrates. Evolution 38, 314-326.
9. Black, R. (1976). The effects of grazing by the limpet, Acmaea insessa, on the kelp, Egregia laevigata, in the intertidal zone. Ecology 57, 265-277.
10. Blanchette, C. A. (1997). Size and survival of intertidal plants in response to wave action: a case study with Fucus gardneri. Ecology 78, 1563-1578.
11. Boller, M. L. and Carrington, E. (2006a). In situ measurements of hydrodynamic forces imposed on Chondrus crispus Stackhouse. J. Exp. Mar. Biol. Ecol. 337, 159-170.
12. Boller, M. L. and Carrington, E. (2006b). The hydrodynamic effects of shape and size change during reconfiguration of a flexible macroalga. J. Exp. Biol. 209, 1894-1903.
13. Bowman, S. M., Keaveny, T. M., Gibson, L. J., Hayes, W. C. and McMahon, T. A. (1994). Compressive creep behavior of bovine trabecular bone. J. Biomech. 27, 301-310.
14. Bowman, S. M., Guo, X. E., Cheng, D. W., Keaveny, T. M., Gibson, L. J., Hayes, W. C. and McMahon, T. A. (1998). Creep contributes to the fatigue behavior of bovine trabecular bone. J. Biomech. Eng. 120, 647-654.
15. Buchanan, C. I. and Marsh, R. L. (2001). Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. J. Appl. Physiol. 90, 164-171.
16. Buschmann, A. H., Correa, J. A., Beltrán, J. and Retamales, C. A. (1997). Determinants of disease expression and survival of infected individual fronds in wild populations of Mazzaella laminarioides (Rhodophyta) in central and southern Chile. Mar. Ecol. Prog. Ser. 154, 269-280.
17. Caler, W. E. and Carter, D. R. (1989). Bone creep-fatigue damage accumulation. J. Biomech. 22, 625-635.
18. Carrington, E. (1990). Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing. J. Exp. Mar. Biol. Ecol. 139, 185-200.
19. Carrington, E., Grace, S. P. and Chopin, T. (2001). Life history phases and the biomechanical properties of the red alga Chondrus crispus (Rhodophyta). J. Phycol. 37, 699-704.
20. Carter, D. R. and Caler, W. E. (1983). Cycle-dependent and time-dependent bone fracture with repeated loading. J. Biomech. Eng. 105, 166-170.
21. Carter, D. R. and Caler, W. E. (1985). A cumulative damage model for bone fracture. J. Orthop. Res. 3, 84-90.
22. Choi, K. and Goldstein, S. A. (1992). A comparison of the fatigue behavior of human trabecular and cortical bone tissue. J. Biomech. 25, 1371-1381.
23. Chopin, T., Kerin, B. F. and Mazerolle, R. (1999). Phycocolloid chemistry as a taxonomie indicator of phylogeny in the Gigartinales, Rhodophyceae: a review and current developments using Fourier transform infrared diffuse reflectance spectroscopy. Phycol. Res. 47, 167-188.
24. Correa, J. A., Flores, V. and Garrido, J. (1994). Green patch disease in lridaea laminarioides (Rhodophyta) caused by Endophyton sp. (Chlorophyta). Dis. Aquat. Org. 19, 203-213.
25. Craigie, J. S. (1990). Cell walls. In Biology of the Red Algae (ed. K. M. Cole and R. G. Sheath), pp. 221-257. Cambridge: Cambridge University Press.
26. Denny, M. W. (2006). Ocean waves, nearshore ecology, and natural selection. Aquat. Ecol. 40, 439-461.
27. Denny, M. and Gaylord, B. (2002). The mechanics of wave-swept algae. J. Exp. Biol. 205, 1355-1362.
28. Denny, M. and Wethey, D. (2001). Physical processes that generate patterns in marine communities. In Marine Community Ecology (ed. M. D. Bertness, S. D. Gaines, and M. E. Hay), pp. 3-37. Sunderland: Sinauer Associates.
29. Denny, M. W., Daniel, T. L. and Koehl, M. A. R. (1985). Mechanical limits to size in wave-swept organisms. Ecol. Monogr. 55, 69-102.
30. Denny, M., Brown, V., Carrington, E., Kraemer, G. and Miller, A. (1989). Fracture mechanics and the survival of wave-swept macroalgae. J. Exp. Mar. Biol. Ecol. 127, 211-228.
31. Denny, M. W., Gaylord, B. P. and Cowen, E. A. (1997). Flow and flexibility: II. The roles of size and shape in determining wave forces on the bull kelp Nereocystis luetkeana. J. Exp. Biol. 200, 3165-3183.
32. Dethier, M. N. (1981). Heteromorphic algal life histories: the seasonal pattern and response to herbivory of the brown crust, Ralfsia californica. Oecologia 49, 333-339.
33. DeWreede, R. E. and Green, L. G. (1990). Patterns of gametophyte dominance of lridaea splendens (Rhodophyta) in Vancouver Harbour, Vancouver, British Columbia, Canada. J. Appl. Phycol. 2, 27-34.
34. Dudgeon, S. R. and Johnson, A. S. (1992). Thick vs. thin: thallus morphology and tissue mechanics influence differential drag and dislodgment of two co-dominant seaweeds. J. Exp. Mar. Biol. Ecol. 165, 23-43.
35. Dudgeon, S. R., Steneck, R. S., Davison, I. R. and Vadas, R. L. (1999). Coexistence of similar species in a space-limited intertidal zone. Ecol. Monogr. 69, 331-352.
36. Dyck, L. J. and DeWreede, R. E. (1995). Patterns of seasonal demographic change in the alternate isomorphic stages of Mazzaella splendens (Gigartinales, Rhodophyta). Phycologia 34, 390-395.
37. Dyck, L. J. and DeWreede, R. E. (2006a). Reproduction and survival in Mazzaella splendens (Gigartinales, Rhodophyta). Phycologia 45, 302-310.
38. Dyck, L. J. and DeWreede, R. E. (2006b). Seasonal and spatial patterns of population density in the marine macroalga Mazzaella splendens (Gigartinales, Rhodophyta). Phycol. Res. 54, 21-31.
39. Dyck, L., DeWreede, R. E. and Garbary, D. (1985). Life history phases in lridaea cordata (Gigartinaceae): relative abundance and distribution from British Columbia to California. Jap. J. Phycol. 33, 225-232.
40. Faugeron, S., Martinez, E. A., Sánchez, P. A. and Correa, J. A. (2000). Infectious diseases in Mazzaella laminarioides (Rhodophyta): estimating the effect of infections on host reproductive potential. Dis. Aquat. Org. 42, 143-148.
41. Foster, M. S. (1982). Factors controlling the intertidal zonation of lridaea flaccida (Rhodophyta). J. Phycol. 18, 285-294.
42. Friedland, M. T. and Denny, M. W. (1995). Surviving hydrodynamic forces in a wave-swept environment: consequences of morphology in the feather boa kelp, Egregia menziesii (Turner). J. Exp. Mar. Biol. Ecol. 190, 109-133.
43. Gaylord, B. (1999). Detailing agents of physical disturbance: wave-induced velocities and accelerations on a rocky shore. J. Exp. Mar. Biol. Ecol. 239, 85-124.
44. Gaylord, B. (2000). Biological implications of surf-zone flow complexity. Limnol. Oceanogr. 45, 174-188.
45. Gaylord, B. and Denny, M. W. (1997). Flow and flexibility: I. Effects of size, shape and stiffness in determining wave forces on the stipitate kelps Eisenia arbórea and Pterygophora californica. J. Exp. Biol. 200, 3141-3164.
46. Gaylord, B., Blanchette, C. A. and Denny, M. W. (1994). Mechanical consequences of size in wave-swept algae. Ecol. Monogr. 64, 287-313.
47. Griffith, A. A. (1921). The phenomena of rupture and flow in solids. Philos. Trans. R. Soc. Lond, A 221, 163-198.
48. Hale, B. (2001). Macroalgal materials: foiling fracture and fatigue from fluid forces. PhD Thesis, Stanford University, Stanford, CA, USA.
49. HAnsen, J. E. (1977). Ecology and natural history of lridaea cordata (Gigartinales, Rhodophyta) growth. J. Phycol. 13, 395-402.
50. Hansen, J. E. and Doyle, W. T. (1976). Ecology and natural history of lridaea cordata (Rhodophyta; Gigartinaceae): population structure. J. Phycol. 12, 273-278.
51. Hawes, I. and Smith, R. (1995). Effect of current velocity on the detachment of thalii of Uiva lactuca (Chlorophyta) in a New Zealand estuary. J. Phycol. 31, 875-880.
52. Hayashi, K. (1996). Biomechanical studies of the remodeling of knee joint tendons and ligaments. J. Biomech. 29, 707-716.
53. Hearle, J. W. S. (1967). Fatigue in fibres and plastics (a review). J. Mater. Sci. 2, 474-488.
54. Helmuth, B. and Denny, M. W. (2003). Predicting wave exposure in the rocky intertidal zone: do bigger waves always lead to larger forces? Limnol. Oceanogr. 48, 1338-1345.
55. Hin, T. S. and Cherry, B. W. (1984). Creep rupture of a linear polyethylene: 1. Rupture and pre-rupture phenomena. Polymer 25, 727-734.
56. Hughes, J. S. and Otto, S. P. (1999). Ecology and the evolution of biphasic life cycles. Am. Nat. 154, 306-320.
57. Johnson, A. S. (2001). Drag, drafting, and mechanical interactions in canopies of the red alga Chondrus crispus. Biol. Bull. 201, 126-135.
58. Johnson, A. S. and Koehl, M. A. R. (1994). Maintenance of dynamic strain similarity and environmental stress factor in different flow habitats: thallus allometry and material properties of a giant kelp. J. Exp. Biol. 195, 381-410.
59. Ker, R. F. (1999). The design of soft collagenous load-bearing tissues. J. Exp. Biol. 202, 3315-3324.
60. Ker, R. F. (2007). Mechanics of tendon, from an engineering perspective. Int. J. Fatigue 29, 1001-1009.
61. Ker, R. F. (2008). Damage and fatigue. In Collagen: Structure and Mechanics (ed. P. Fratzl), pp. 111 -131. New York: Springer Science and Business Media.
62. Ker, R. F., Wang, X. T. and Pike, A. V. L. (2000). Fatigue quality of mammalian tendons. J. Exp. Biol. 203, 1317-1327.
63. Kitzes, J. A. and Denny, M. W. (2005). Red algae respond to waves: morphological and mechanical variation in Mastocarpus papillatus along a gradient of force. Biol. Bull. 208, 114-119.
64. Kloareg, B. and Quatrano, R. S. (1988). Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr. Mar. Biol. Annu. Rev. 26, 259-315.
65. Klompen, E. T. J., Engels, T. A. P., van Breemen, L. C. A., Schreurs, P. J. G., Govaert, L. E. and Meijer, H. E. H. (2005). Quantitative prediction of long-term failure of polycarbonate. Macromolecules 38, 7009-7017.
66. Koehl, M. A. R. (1984). How do benthic organisms withstand moving water? Am. Zool. 24, 57-70.
67. Koehl, M. A. R. (1986). Seaweeds in moving water: form and mechanical function. In On the Economy of Plant Form and Function (ed. T. J. Givnish), pp. 603-634. Cambridge: Cambridge University Press.
68. Koehl, M. A. R. and Alberte, R. S. (1988). Flow, flapping, and photosynthesis of Nereocystis luetkeana: a functional comparison of undulate and flat blade morphologies. Mar. Biol. 99, 435-444.
69. Kraemer, G. P. and Chapman, D. J. (1991). Biomechanics and alginic acid composition during hydrodynamic adaptation by Egregia menziesii (Phaeophyta) juveniles. J. Phycol. 27, 47-53.
70. Littler, M. M. and Littler, D. S. (1980). The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am. Nat. 116, 25-44.
71. Littler, M. M. and Littler, D. S. (1983). Heteromorphic life-history strategies in the brown alga Scytosiphon lomentaria (Lyngb.) Link. J. Phycol. 19, 425-431.
72. Lubchenco, J. and Cubit, J. (1980). Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology 61, 676-687.
73. Mach, K. J., Nelson, D. V. and Denny, M. W. (2007a). Review: techniques for predicting the lifetimes of wave-swept macroalgae: a primer on fracture mechanics and crack growth. J. Exp. Biol. 210, 2213-2230.
74. Mach, K. J., Hale, B. B., Denny, M. W. and Nelson, D. V. (2007b). Death by small forces: a fracture and fatigue analysis of wave-swept macroalgae. J. Exp. Biol. 210, 2231-2243.
75. Martin, R. B. (2003). Fatigue microdamage as an essential element of bone mechanics and biology. Calcif. Tissue Int. 73, 101-107.
76. Martone, P. T. and Denny, M. W. (2008). To break a coralline: mechanical constraints on the size and survival of a wave-swept seaweed. J. Exp. Biol. 211, 3433-3441.
77. Miller, L. P. and Gaylord, B. (2007). Barriers to flow: the effects of experimental cage structures on water velocities in high-energy subtidal and intertidal environments. J. Exp. Mar. Biol. Ecol. 344, 215-228.
78. Milligan, K. L. D. and DeWreede, R. E. (2000). Variations in holdfast attachment mechanics with developmental stage, substratum-type, season, and wave-exposure for the intertidal kelp species Hedophyllum sessile (C. Agardh) Setchell. J. Exp. Mar. Biol. Ecol. 254, 189-209.
79. Nalla, R. K., Imbeni, V., Kinney, J. H., Staninec, M., Marshall, S. J. and Ritchie, R. O. (2003). In vitro fatigue behavior of human dentin with implications for life prediction. J. Biomed. Mater. Res. 66A, 10-20.
80. Nalla, R. K., Kruzic, J. J., Kinney, J. H. and Ritchie, R. O. (2005). Aspects of in vitro fatigue in human cortical bone: time and cycle dependent crack growth. Biomaterials 26, 2183-2195.
81. Norton, T. A., Mathieson, A. C. and Neushul, M. (1981). Morphology and environment. In The Biology of Seaweeds (ed. C. S. Lobban and M. J.Wynne), pp. 421-451. Berkeley, CA: University of California Press.
82. Noyes, F. R. (1977). Functional properties of knee ligaments and alterations induced by immobilization: a correlative biomechanical and histological study in primates. Clin. Orthop. Relat. Res. 123, 210-242.
83. O'Brien, F. J., Taylor, D. and Lee, T. C. (2003). Microcrack accumulation at different intervals during fatigue testing of compact bone. J. Biomech. 36, 973-980.
84. Pike, A. V. L., Ker, R. F. and Alexander, R. M. (2000). The development of fatigue quality in high- and low-stressed tendons of sheep (Ovis aries). J. Exp. Biol. 203, 2187-2193.
85. Pratt, M. C. and Johnson, A. S. (2002). Strength, drag, and dislodgment of two competing intertidal algae from two wave exposures and four seasons. J. Exp. Mar. Biol. Ecol. 272, 71-101.
86. Roff, D. A. (1992). The Evolution of Life Histories: Theory and Analysis. New York: Chapman & Hall.
87. Schechtman, H. and Bader, D. L. (1997). In vitro fatigue of human tendons. J. Biomech. 30, 829-835.
88. Scrosati, R. and DeWreede, R. E. (1999). Demographic models to simulate the stable ratio between ecologically similar gametophytes and tetrasporophytes in populations of the Gigartinaceae (Rhodophyta). Phycol. Res. 47, 153-157.
89. Seymour, R. J., Tegner, M. J., Dayton, P. K. and Parnell, P. E. (1989). Storm wave induced mortality of giant kelp, Macrocystis pyrifera, in Southern California. Estuar. Coast. Shelf Sci. 28, 277-292.
90. Shaughnessy, F. J. and DeWreede, R. E. (2001). Size, survival and the potential for reproduction in transplants of Mazzaella splendens and M. linearis (Rhodophyta). Mar. Ecol. Prog. Ser. 222, 109-118.
91. Shaughnessy, F. J., DeWreede, R. E. and Bell, E. C. (1996). Consequences of morphology and tissue strength to blade survivorship of two closely related Rhodophyta species. Mar. Ecol. Prog. Ser. 136, 257-266.
92. Slocum, C. J. (1980). Differential susceptibility to grazers in two phases of an intertidal alga: advantages of heteromorphic generations. J. Exp. Mar. Biol. Ecol. 46, 99-110.
93. Sprugel, D. G. (1983). Correcting for bias in log-transformed allometric equations. Ecology 64, 209-210.
94. Stephens, R. I., Fatemi, A., Stephens, R. R. and Fuchs, H. O. (2001). Metal Fatigue in Engineering. 2nd edn. New York: J. Wiley.
95. Taylor, D., Hazenberg, J. G. and Lee, T. C. (2007). Living with cracks: damage and repair in human bone. Nat. Mater. 6, 263-268.
96. Tomanek, L. and Helmuth, B. (2002). Physiological ecology of rocky intertidal organisms: a synergy of concepts. Int. Comp. Biol. 42, 771-775.
97. Utter, B. D. and Denny, M. W. (1996). Wave-induced forces on the giant kelp Macrocystis pyrifera (Agardh): field test of a computational model. J. Exp. Biol. 199, 2645-2654.
98. Vogel, S. (1984). Drag and flexibility in sessile organisms. Am. Zool. 24, 37-44.
99. Wang, X. T. and Ker, R. F. (1995). Creep rupture of wallaby tail tendons. J. Exp. Biol. 198, 831-845.
100. Wang, X. T., Ker, R. F. and Alexander, R. M. (1995). Fatigue rupture of wallaby tail tendons. J. Exp. Biol. 198, 847-852.
101. Woo, S. L. Y., Gomez, M. A., Sites, T. J., Newton, P. O., Orlando, C. A. and Akeson, W. H. (1987). The biomechanical and morphological changes in the medial collateral ligament of the rabbit after immobilization and remobilization. J. Bone Joint Surg. 69-A, 1200-1211.
102. Wren, T. A. L., Lindsey, D. P., Beaupré, G. S. and Carter, D. R. (2003). Effects of creep and cyclic loading on the mechanical properties and failure of human Achilles tendon. Ann. Biomed. Eng. 31, 710-717.
103. Zioupos, P. and Currey, J. D. (1994). The extent of microcracking and the morphology of microcracks in damaged bone. J. Mater. Sci. 29, 978-986.
104. Zioupos, P., Wang, X. T. and Currey, J. D. (1996). The accumulation of fatigue microdamage in human cortical bone of two different ages. Clin. Biomech. 11, 365-375.
105. Zioupos, P., Currey, J. D. and Casinos, A. (2001). Tensile fatigue in bone: are cycles, or time to failure, or both, important? J. Theor. Biol. 210, 389-399.