Historical baselines and the future of shell calcification for a foundation species in a changing ocean

Abstract

Seawater pH and the availability of carbonate ions are decreasing due to anthropogenic carbon dioxide emissions, posing challenges for calcifying marine species. Marine mussels are of particular concern given their role as foundation species worldwide. Here, we document shell growth and calcification patterns in Mytilus californianus, the California mussel, over millennial and decadal scales. By comparing shell thickness across the largest modern shells, the largest mussels collected in the 1960s-1970s and shells from two Native American midden sites ( 1000-2420 years BP), we found that modern shells are thinner overall, thinner per age category and thinner per unit length. Thus, the largest individuals of this species are calcifying less now than in the past. Comparisons of shell thickness in smaller individuals over the past 10-40 years, however, do not show significant shell thinning. Given our sampling strategy, these results are unlikely to simply reflect within-site variability or preservation effects. Review of environmental and biotic drivers known to affect shell calcification suggests declining ocean pH as a likely explanation for the observed shell thinning. Further future decreases in shell thickness could have significant negative impacts on M. californianus survival and, in turn, negatively impact the species-rich complex that occupies mussel beds.

A mineralogical record of ocean change: Decadal and centennial patterns in the California mussel

“…Excavation of Native American middens from the Makah Tribe (McMillan, ), who used Tatoosh Island as a summer camp prior to the 1800s and historically had a large settlement at Sand Point, provided ‘midden’ valves from Tatoosh Island through the Makah Cultural and Resource Center, while Sand Point midden material was provided by the Olympic National Park. These shells were radiocarbon dated using shell material from their most recent year of growth, with Tatoosh Island midden shells dated to 1000–1340 years BP in 2010 (Pfister et al., ) and Sand Point midden shells dated to 2150–2440 years BP in 2015 (Pfister et al., ). Valves were cross‐sectioned along their axis of maximum growth using a slow‐speed saw with a diamond blade to make a 3 mm‐thick cross‐section.…”

“…Previous work has shown that the thickness of annual growth bands within the inner prismatic layer of M. californianus is reduced by approximately half when comparing modern day specimens to shells dated to 1000–1340 years BP at Tatoosh Island, WA (Pfister et al., ), suggesting that modern shells may be experiencing stress associated with biomineralization through time. Here, we present a study of shell structure from the California mussel, M. californianus , spanning decadal and centennial scales to determine the long‐term effects of changes in ocean carbon chemistry on shell mineralogy in a natural system.…”

“…Current uncertainty regarding organismal responses to ongoing climate changes deals with the juxtaposed issues of scale and mechanism: laboratory studies enable the isolation of a specific stressor, while field studies are necessary to truly understand effects of a stressor in a natural, often more variable, system. While field studies also can detect long‐term evolutionary or population dynamics (Hofmann et al., ; Pfister et al., ), the length of time required to see a response can be prohibitive. Organisms that retain growth history records over millennial timescales and that are relevant to contemporary environmental stressors offer a model to overcome the challenge of long‐term ecological relevance (Cobb, Charles, Cheng, & Edwards, ; Halfar, Adey, & Kronz, ; Mann et al., ).…”

“…Calcification can be affected by multiple environmental parameters, including pCO 2 (Fitzer, Cusack, Phoenix, & Kamenos, ; Gazeau et al., ; Kroeker, Kordas, Crim, & Singh, ; Pfister et al., ), temperature (Fitzer et al., ), wave exposure (Fox & Coe, ), food availability (Coe, ; Hahn et al., ; Thomsen & Melzner, ; Waldbusser et al., ), predation pressure (Vermeij, ), and their interacting effects (Kroeker, Kordas, & Harley, ; Melzner et al., ). These calcification responses include changes in growth rate and overall size (Thomsen & Melzner, ), changes in shell morphology (Fitzer et al., ; Pfister et al., ), and mineralogical plasticity (Nash et al., ; Pauly, Kamenos, Donohue, & LeDrew, ). Mineralogical plasticity has been proposed as a potentially beneficial adaptive mechanism (Fitzer et al., ; Leung, Russell, & Connell, ) that allows calcified organisms to continue growth under acidified conditions.…”

Explaining Ocean Warming: Causes, scale, effects and consequences

“…Reduced pH can affect metabolism and energy budgets in marine organisms, particularly in organisms that produce calcium carbonate for shells or skeletons (Kroeker et al, 2010;Harvey et al, 2013Harvey et al, , 2016. For example, calcification rates in Mytilus californianus mussels in Washington State, USA, have decreased significantly, probably due to declining pH (Pfister et al, 2016). Mussel beds are the dominant space occupier of many temperate rocky shore coastlines around the planet.…”