Metabolic cost of calcification in bivalve larvae under experimental ocean acidification

Frieder, Christina A.; Applebaum, Scott L.; Pan, T.-C. Francis; Hedgecock, Dennis; Manahan, Donal T.

doi:10.1093/icesjms/fsw213

Cited by 74 publications

(55 citation statements)

References 67 publications

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“…Furthermore, experimental work has directly measured the metabolic carbon content of larval oyster shells [ Waldbusser et al , ], which is a property directly linked to kinetic constraints in our model. Our derived costs agree well with values obtained experimentally [ Palmer , ; Waldbusser et al , ; Frieder et al , ].…”

Section: Introductionsupporting

confidence: 89%

“…More recent investigations have increasingly focused on acidification stress experienced during early ontogenetic stages, the larvae and juveniles [Albright et al, 2010;Waldbusser et al, 2013Waldbusser et al, , 2015aWaldbusser et al, , 2015bWaldbusser et al, , 2016Frieder et al, 2016;Bylenga et al, 2017]. These earlier life stages experience two additional physiological constraints when compared to their adult forms.…”

Section: Global Biogeochemical Cyclesmentioning

confidence: 99%

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Energetic costs of calcification under ocean acidification

Spalding

Finnegan

Fischer

2017

Global Biogeochemical Cycles

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Anthropogenic ocean acidification threatens to negatively impact marine organisms that precipitate calcium carbonate skeletons. Past geological events, such as the Permian‐Triassic Mass Extinction, together with modern experiments generally support these concerns. However, the physiological costs of producing a calcium carbonate skeleton under different acidification scenarios remain poorly understood. Here we present an idealized mathematical model to quantify whole‐skeleton costs, concluding that they rise only modestly (up to ∼10%) under acidification expected for 2100. The modest magnitude of this effect reflects in part the low energetic cost of inorganic, calcium carbonate relative to the proteinaceous organic matrix component of skeletons. Our analysis does, however, point to an important kinetic constraint that depends on seawater carbonate chemistry, and we hypothesize that the impact of acidification is more likely to cause extinctions within groups where the timescale of larval development is tightly constrained. The cheapness of carbonate skeletons compared to organic materials also helps explain the widespread evolutionary convergence upon calcification within the metazoa.

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Section: Introductionsupporting

confidence: 89%

Section: Global Biogeochemical Cyclesmentioning

confidence: 99%

Energetic costs of calcification under ocean acidification

Spalding

Finnegan

Fischer

2017

Global Biogeochemical Cycles

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“…Unhindered protein synthesis under low pH conditions has been observed in C. gigas (Frieder et al, 2016) and maintenance of translation-related proteins may be further evidence that ocean acidification does not impact this essential process. At day 8, the molecular developmental signals were still diverged between the two pH treatments, with an increase in abundance of DNA replication and translation proteins at pH 7.1.…”

Section: Development At Ph 71mentioning

confidence: 92%

“…In fact, metamorphosis in geoduck is known to be delayed by stress (Goodwin & Pease, 1989) and low pH (Huo et al, 2019). Developmental delay due to ocean acidification has been observed in other bivalve larvae, such as C. gigas and M. galloprovincialis (De Wit, Durland, Ventura, & Langdon, 2018;Frieder et al, 2016;Kurihara et al, 2008;Timmins-Schiffman et al, 2013). It is also possible that the larger size and faster development at pH 7.5 were due in part to greater mortality rate at the higher pH, possibly releasing constraints of density effects on larval size.…”

Section: Development At Ph 71mentioning

confidence: 99%

Dynamic response in the larval geoduck (Panopea generosa) proteome to elevated pCO₂

Timmins‐Schiffman

Guzmán

Thompson

et al. 2019

Ecology and Evolution

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Pacific geoducks (Panopea generosa) are clams found along the northeast Pacific coast where they are important components of coastal and estuarine ecosystems and a major aquaculture product. The Pacific coastline, however, is also experiencing rapidly changing ocean habitat, including significant reductions in pH. To better understand the physiological impact of ocean acidification on geoduck clams, we characterized for the first time the proteomic profile of this bivalve during larval development and compared it to that of larvae exposed to low pH conditions. Geoduck larvae were reared at pH 7.5 (ambient) or pH 7.1 in a commercial shellfish hatchery from day 6 to day 19 postfertilization and sampled at six time points for an in‐depth proteomics analysis using high‐resolution data‐dependent analysis. Larvae reared at low pH were smaller than those reared at ambient pH, especially in the prodissoconch II phase of development, and displayed a delay in their competency for settlement. Proteomic profiles revealed that metabolic, cell cycle, and protein turnover pathways differed between the two pH and suggested that differing phenotypic outcomes between pH 7.5 and 7.1 are likely due to environmental disruptions to the timing of physiological events. In summary, ocean acidification results in elevated energetic demand on geoduck larvae, resulting in delayed development and disruptions to normal molecular developmental pathways, such as carbohydrate metabolism, cell growth, and protein synthesis.

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“…Given the number of unique transcripts differentially expressed and the magnitude of expression, scallop larvae presumably invest significant amounts of energy into cellular defense when exposed to C. polykrikoides . Even under ideal conditions, large amounts of energy are required by bivalve larvae to precipitate their initial shell (e.g., <48 hr; Waldbusser et al, ; Frieder, Applebaum, Pan, Hedgecock, & Manahan, ). Hence, responses elicited by C. polykrikoides may exhaust energy reserves within rapidly developing larvae contributing to their mortality.…”

Section: Discussionmentioning

confidence: 99%

The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors

Griffith

Harke

DePasquale

et al. 2019

Ecology and Evolution

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Global ocean change threatens marine life, yet a mechanistic understanding of how organisms are affected by specific stressors is poorly understood. Here, we identify and compare the unique and common transcriptomic responses of an organism experiencing widespread fisheries declines, Argopecten irradians (bay scallop) exposed to multiple stressors including high p CO 2 , elevated temperature, and two species of harmful algae, Cochlodinium (aka Margalefidinium ) polykrikoides and Aureococcus anophagefferens using high‐throughput sequencing (RNA‐seq). After 48 hr of exposure, scallop transcriptomes revealed distinct expression profiles with larvae exposed to harmful algae ( C. polykrikoides and A. anophagefferens ) displaying broader responses in terms of significantly and differentially expressed (DE) transcripts (44,922 and 4,973; respectively) than larvae exposed to low pH or elevated temperature (559 and 467; respectively). Patterns of expression between larvae exposed to each harmful algal treatment were, however, strikingly different with larvae exposed to A. anophagefferens displaying large, significant declines in the expression of transcripts ( n = 3,615; 87% of DE transcripts) whereas exposure to C. polykrikoides increased the abundance of transcripts, more than all other treatments combined ( n = 43,668; 97% of DE transcripts). Larvae exposed to each stressor up‐regulated a common set of 21 genes associated with protein synthesis, cellular metabolism, shell growth, and membrane transport. Larvae exposed to C. polykrikoides displayed large increases in antioxidant‐associated transcripts, whereas acidification‐exposed larvae increased abundance of transcripts associated with shell formation. After 10 days of exposure, each harmful algae caused declines in survival that were significantly greater than all other treatments. Collectively, this study reveals the common and unique transcriptional responses of bivalve larvae to stressors that promote population declines within coastal zones, providing insight into the means by which they promote mortality as well as traits possessed by bay scallops that enable potential resistance.

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Metabolic cost of calcification in bivalve larvae under experimental ocean acidification

Cited by 74 publications

References 67 publications

Energetic costs of calcification under ocean acidification

Energetic costs of calcification under ocean acidification

Dynamic response in the larval geoduck (Panopea generosa) proteome to elevated pCO₂

The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors

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Metabolic cost of calcification in bivalve larvae under experimental ocean acidification

Cited by 74 publications

References 67 publications

Energetic costs of calcification under ocean acidification

Energetic costs of calcification under ocean acidification

Dynamic response in the larval geoduck (Panopea generosa) proteome to elevated pCO2

The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors

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Dynamic response in the larval geoduck (Panopea generosa) proteome to elevated pCO₂