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

Abstract

The biomechanics of specialized mechanical structures produced by organisms provides crucial fitness advantages. The energetic cost associated with producing these structural materials and the resulting energetic trade‐off with growth, however, is rarely quantified. We integrate resource allocation to structural material production with an energetic framework by combining an experimental manipulation with an energetic model. Mytilid bivalves produce byssus, a network of collagen‐like threads that tethers individuals to hard substrate. We hypothesized that a manipulation that induces the production of more byssal threads would result in increased energetic cost and decreased growth of the species Mytilus trossulus. In month‐long field experiments in spring and autumn, we severed byssal threads across a range of frequencies (never, weekly, daily), and measured shell and tissue growth. We then quantified the costs associated with the production of byssal threads using a Scope for Growth model. We found that byssal thread removal increased byssal thread production and decreased growth. The cost calculated per byssal thread was similar in the spring and autumn (~1 J/thread), but energy budget calculations differed by season, and depended on thread quantity and seasonal differences in assumptions of metabolic costs. This work demonstrates that the cost of producing a structural material has a substantial effect on mussel energetic state. The energetic cost of producing byssal threads was 2%–8% percent of the energy budget in control groups that had low byssal thread production, and increased six to 11‐fold (up to 47%) in mussels induced to produce threads daily. We propose that characterizing the trade‐off between the cost of biomaterial production and growth has implications for understanding the role of trade‐offs in adaptive evolution, and improved natural resource management and conservation practices. A free Plain Language Summary can be found within the Supporting Information of this article.

Mussels Repair Shell Damage despite Limitations Imposed by Ocean Acidification

“…Additionally, the decline in physiological condition of mussels within all laboratory treatments supports the conclusion that shell repair is energy-intensive. Given its importance to survival across a wide range of molluscan species, shell repair may impose energetic limitations on other physiological processes such as growth or reproduction [103]. Our results suggest that in areas where bivalves sustain a high rate of shell damage, it is possible that the costs associated with shell repair could compound over time, preventing smaller individuals from quickly surpassing the size range in which larger predators (e.g., sea stars, crustaceans) can handle them [104].…”

Mussels repair shell damage despite limitations imposed by ocean acidification

“…Biomineralization is an energy intensive process [85,86], and the added cost of shell repair (maintenance) could impose energetic limitations on other physiological processes such as growth or reproduction [87]. In areas where mussels sustain a high rate of shell damage, it is possible that the cost associated with shell repair could compound over time, preventing smaller individuals from quickly surpassing the size range in which larger predators (e.g., sea stars, crustaceans) can handle them [88].…”

Mussel Byssal Attachment Weakened by Anthropogenic Noise

“…The noise-induced decline in byssal thread production (i.e., the decrease in the diameter and volume of byssal thread, and the down-regulation of genes encoding structural proteins of byssal thread) might be due to limited energy availability. It has been shown that the energetic cost of byssal thread production is substantial, requiring 8-10% of a mussel's total energy expenditure (Hawkins and Bayne, 1985;Lurman et al, 2013;Roberts et al, 2021). However, studies have suggested that anthropogenic noise adversely affected the feeding behavior and metabolism activity of marine bivalves, including mussels, which seems to result in energy deficiency (Peng et al, 2016;Spiga et al, 2016;Shi et al, 2019;Wale et al, 2019;Vazzana et al, 2020).…”