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.

Resource allocation to a structural biomaterial: Induced production of byssal threads decreases growth of a marine mussel

“…The energetic trade‐off between thread production and tissue growth can be characterized with a SFG model (Figure 1). Mussels modulate their production of byssal threads in response to a range of environmental conditions, such as increased wave disturbance (Bell & Gosline, 1997; Carrington et al., 2008; Dolmer & Svane, 1994; Lee et al., 1990; Moeser et al., 2006; Van Winkle, 1970; Young, 1985), seawater temperature and pH (George et al., 2018; Newcomb et al., 2019; O’Donnell et al., 2013), as well as seasonal and/or reproductive cycles in natural systems (Carrington, 2002; Moeser & Carrington, 2006; Newcomb, 2015; Zardi et al., 2007). Within the framework of a SFG model, the theoretical variable, SFG, can be used an index of tissue growth (including gonadal and somatic tissue growth), and is calculated as the difference between consumption minus physiological cost (Bayne et al., 1976; Sebens, 2002; Widdows & Bayne, 1971; Figure 1).…”

­Blue mussel (Mytilus spp.) cultivation in mesohaline eutrophied inner coastal waters: mitigation potential, threats and cost effectiveness

“…Especially, in shallow coastal waters with limited water exchange rates high water temperatures can appear during summer. Fly and Hilbish (2013) stated that the energetic balance of M. trossulus is affected by water temperatures above 17 • C. Other studies have shown that byssus threads are up to 60% weaker at water temperatures of 25 • C than at 10 • C (Newcomb et al, 2019). Westerbom et al (2019) concluded that temperature stress coupled with continuous salinity stress may also cause increased mortality.…”

“…Fly and Hilbish (2013) stated that the energetic balance of M. trossulus is affected by water temperatures above 17 °C. Other studies have shown that byssus threads are up to 60% weaker at water temperatures of 25 °C than at 10 °C ( Newcomb et al, 2019 ). Westerbom et al.…”

Resilience of cold water aquaculture: a review of likely scenarios as climate changes in the Gulf of Maine

“…Larval growth, calcification rates and overall health of M. edulis will be inhibited during this same time period (Gazeau et al 2007;Beesley et al 2008;Gazeau et al 2010), but several studies (Beesley et al 2008;Thomsen & Melzner, 2010;Dickey et al 2018) suggest that M. edulis metabolism, tissue condition and thread production will not be affected. In contrast, studies with Mytilus trossulus (Gould 1850) on the U.S. Washington coast found that byssal thread number and attachment strength were negatively affected by higher temperature (25°C versus 10°C) and secreted adhesives did not cure well at pH < 8 (O'Donnell et al 2013; George & Carrington 2018;Newcomb et al 2019). Mytilus trossulus also occurs in Maine (especially in Bioregion 3), suggesting the usefulness of additional studies of adhesive plaques and thread strength in Maine for both M. edulis and M. trossulus, because failure of these structures due to climate change could have significant negative implications for mussel aquaculture.…”

“…2013; George & Carrington 2018; Newcomb et al . 2019). Mytilus trossulus also occurs in Maine (especially in Bioregion 3), suggesting the usefulness of additional studies of adhesive plaques and thread strength in Maine for both M. edulis and M. trossulus , because failure of these structures due to climate change could have significant negative implications for mussel aquaculture.…”