Only as strong as the weakest link: structural analysis of the combined effects of elevated temperature and pCO2 on mussel attachment

Abstract Predicting how combinations of stressors will affect failure risk is a key challenge for the field of ecomechanics and, more generally, ecophysiology. Environmental conditions often influence the manufacture and durability of biomaterials, inducing structural failure that potentially compromises organismal reproduction, growth, and survival. Species known for tight linkages between structural integrity and survival include bivalve mussels, which produce numerous byssal threads to attach to hard substrate. Among the current environmental threats to marine organisms are ocean warming and acidification. Elevated pCO2 exposure is known to weaken byssal threads by compromising the strength of the adhesive plaque. This study uses structural analysis to evaluate how an additional stressor, elevated temperature, influences byssal thread quality and production. Mussels (Mytilus trossulus) were placed in controlled temperature and pCO2 treatments, and then, newly produced threads were counted and pulled to failure to determine byssus strength. The effects of elevated temperature on mussel attachment were dramatic; mussels produced 60% weaker and 65% fewer threads at 25°C in comparison to 10°C. These effects combine to weaken overall attachment by 64–88% at 25°C. The magnitude of the effect of pCO2 on thread strength was substantially lower than that of temperature and, contrary to our expectations, positive at high pCO2 exposure. Failure mode analysis localized the effect of temperature to the proximal region of the thread, whereas pCO2 affected only the adhesive plaques. The two stressors therefore act independently, and because their respective target regions are interconnected (resisting tension in series), their combined effects on thread strength are exactly equal to the effect of the strongest stressor. Altogether, these results show that mussels, and the coastal communities they support, may be more vulnerable to the negative effects of ocean warming than ocean acidification.

[1]  Ecological mechanics , 2020, Mechanical Design in Organisms.

[2]  Stephen A. Wainwright,et al.  Mechanical Design in Organisms , 2020 .

[3]  E. Carrington,et al.  Microscale pH and Dissolved Oxygen Fluctuations within Mussel Aggregations and Their Implications for Mussel Attachment and Raft Aquaculture , 2019, Journal of Shellfish Research.

[4]  S. Dupont,et al.  Seawater acidification and temperature modulate anti-predator defenses in two co-existing Mytilus species. , 2019, Marine pollution bulletin.

[5]  T. Bowden,et al.  The impact of ocean acidification on the byssal threads of the blue mussel (Mytilus edulis) , 2018, PloS one.

[6]  S. Dupont,et al.  Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—A review , 2018, Global change biology.

[7]  K. Sebens,et al.  Estimation of fitness from energetics and life‐history data: An example using mussels , 2018, Ecology and evolution.

[8]  E. Carrington,et al.  Environmental post-processing increases the adhesion strength of mussel byssus adhesive , 2018, Biofouling.

[9]  Kevin Miklasz,et al.  Macroalgal spore dysfunction: ocean acidification delays and weakens adhesion , 2018, Journal of phycology.

[10]  M. Abad,et al.  Susceptibility of two co-existing mytilid species to simulated predation under projected climate change conditions , 2018, Hydrobiologia.

[11]  A. Zhan,et al.  Influencing Mechanism of Ocean Acidification on Byssus Performance in the Pearl Oyster Pinctada fucata. , 2017, Environmental science & technology.

[12]  R. Feely,et al.  New ocean, new needs: Application of pteropod shell dissolution as a biological indicator for marine resource management , 2017 .

[13]  S. Dupont,et al.  Defense Responses to Short-term Hypoxia and Seawater Acidification in the Thick Shell Mussel Mytilus coruscus , 2017, Front. Physiol..

[14]  M. Dean,et al.  Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication , 2017, Nature Communications.

[15]  Christopher D G Harley,et al.  Embracing interactions in ocean acidification research: confronting multiple stressor scenarios and context dependence , 2017, Biology Letters.

[16]  Yu Han,et al.  Ocean acidification decreases mussel byssal attachment strength and induces molecular byssal responses , 2017 .

[17]  J. Herbert Waite,et al.  Mussel adhesion – essential footwork , 2017, Journal of Experimental Biology.

[18]  F. Chavez,et al.  Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability. , 2016, Ecology letters.

[19]  P. Dubois,et al.  The impact of ocean acidification and warming on the skeletal mechanical properties of the sea urchin Paracentrotus lividus from laboratory and field observations , 2016 .

[20]  J. Stillman,et al.  Multiple Stressors in a Changing World: The Need for an Improved Perspective on Physiological Responses to the Dynamic Marine Environment. , 2016, Annual review of marine science.

[21]  L. Newcomb.  Elevated temperature and ocean acidification alter mechanics of mussel attachment , 2015 .

[22]  J. Hall‐Spencer,et al.  Ocean acidification bends the mermaid's wineglass , 2015, Biology Letters.

[23]  K. Sebens,et al.  Mussels as a model system for integrative ecomechanics. , 2015, Annual review of marine science.

[24]  Sarah Faulwetter,et al.  Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem , 2015, Global change biology.

[25]  E. Carrington,et al.  The effect of water temperature and flow on respiration in barnacles: patterns of mass transfer versus kinetic limitation , 2014, Journal of Experimental Biology.

[26]  A. Ivanina,et al.  Interactive effects of elevated temperature and CO2 levels on energy metabolism and biomineralization of marine bivalves Crassostrea virginica and Mercenaria mercenaria. , 2013, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[27]  M. O'Donnell,et al.  Elevated pCO2 causes developmental delay in early larval Pacific oysters, Crassostrea gigas , 2013 .

[28]  Michael J. O'Donnell,et al.  Mussel byssus attachment weakened by ocean acidification , 2013 .

[29]  Carlos M Duarte,et al.  Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming , 2013, Global change biology.

[30]  L. Talley,et al.  Securing ocean benefits for society in the face of climate change , 2013 .

[31]  R. Feely,et al.  Extensive dissolution of live pteropods in the Southern Ocean , 2012 .

[32]  Joshua S Madin,et al.  Calcification, Storm Damage and Population Resilience of Tabular Corals under Climate Change , 2012, PloS one.

[33]  Waite Jh,et al.  Changing environments and structure--property relationships in marine biomaterials. , 2012 .

[34]  J. Waite,et al.  Changing environments and structure–property relationships in marine biomaterials , 2012, Journal of Experimental Biology.

[35]  B. Gaylord,et al.  Functional impacts of ocean acidification in an ecologically critical foundation species , 2011, Journal of Experimental Biology.

[36]  Scott C. Doney,et al.  The Growing Human Footprint on Coastal and Open-Ocean Biogeochemistry , 2010, Science.

[37]  M. Boller,et al.  Seasonal disturbance to mussel beds: Field test of a mechanistic model predicting wave dislodgment , 2009 .

[38]  E. Carrington,et al.  Interspecific Comparison of the Mechanical Properties of Mussel Byssus , 2006, The Biological Bulletin.

[39]  G. Somero,et al.  Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus) , 2006, Journal of Experimental Biology.

[40]  Emily Carrington,et al.  Seasonal variation in mussel byssal thread mechanics , 2006, Journal of Experimental Biology.

[41]  E. Carrington,et al.  Seasonal influence of wave action on thread production in Mytilus edulis , 2006, Journal of Experimental Biology.

[42]  Joshua S Madin.  Mechanical limitations of reef corals during hydrodynamic disturbances , 2005, Coral Reefs.

[43]  Hanns-Christof Spatz,et al.  Basic biomechanics of self-supporting plants: wind loads and gravitational loads on a Norway spruce tree , 2000 .

[44]  M. Koehl,et al.  Ecological biomechanics of benthic organisms: life history, mechanical design and temporal patterns of mechanical stress. , 1999, The Journal of experimental biology.

[45]  Scott,et al.  A method for the assessment of the risk of wheat lodging , 1998, Journal of theoretical biology.

[46]  R. M. Alexander,et al.  A theory of mixed chains applied to safety factors in biological systems. , 1997, Journal of theoretical biology.

[47]  Gosline,et al.  Mechanical design of mussel byssus: material yield enhances attachment strength , 1996, The Journal of experimental biology.

[48]  Mark W. Denny.  Predicting Physical Disturbance: Mechanistic Approaches to the Study of Survivorship on Wave‐Swept Shores , 1995 .

[49]  Johnson,et al.  MAINTENANCE OF DYNAMIC STRAIN SIMILARITY AND ENVIRONMENTAL STRESS FACTOR IN DIFFERENT FLOW HABITATS: THALLUS ALLOMETRY AND MATERIAL PROPERTIES OF A GIANT KELP , 1994, The Journal of experimental biology.

[50]  Steven Vogel,et al.  Life's Devices: The Physical World of Animals and Plants , 1988 .

[51]  L. Comeau,et al.  Elevated seawater temperature, not pCO2, negatively affects post-spawning adult mussels (Mytilus edulis) under food limitation. , 2018, Conservation physiology.

[52]  Christopher D G Harley,et al.  Ocean acidification through the lens of ecological theory. , 2015, Ecology.

[53]  A. R. Ennos,et al.  Understanding and Reducing Lodging in Cereals , 2004 .

[54]  G. Young.  Byssus-thread production by the mussel Mytilus edulis : effects of environmental factors , 1985 .

[55]  J. P. Riley,et al.  The effect of analytical error on the evaluation of the components of the aquatic carbon-dioxide system , 1978 .