Ocean acidification has the potential to significantly impact both aquaculture and wild-caught mollusk fisheries around the world. In this work, we build upon a previously published integrated assessment model of the US Atlantic Sea Scallop (Placopecten magellanicus) fishery to determine the possible future of the fishery under a suite of climate, economic, biological, and management scenarios. We developed a 4x4x4x4 hypercube scenario framework that resulted in 256 possible combinations of future scenarios. The study highlights the potential impacts of ocean acidification and management for a subset of future climate scenarios, with a high CO 2 emissions case (RCP8.5) and lower CO 2 emissions and climate mitigation case (RCP4.5). Under RCP4.5 and the highest impact and management scenario, ocean acidification has the potential to reduce sea scallop biomass by approximately 13% by the end of century; however, the lesser impact scenarios cause very little change. Under RCP8.5, sea scallop biomass may decline by more than 50% by the end of century, leading to subsequent declines in industry landings and revenue. Management-set catch limits improve the outcomes of the fishery under both climate scenarios, and the addition of a 10% area closure increases future biomass by more than 25% under the highest ocean acidification impacts. However, increased management still does not stop the projected long-term decline of the fishery under ocean acidification scenarios. Given our incomplete understanding of acidification impacts on P. magellanicus, these declines, along with the high value of the industry, suggest population-level effects of acidification should be a clear research priority. Projections described in this manuscript illustrate both the potential impacts of ocean acidification under a business-as-usual and a moderately strong climate-policy scenario. We also illustrate the importance of fisheries management targets in improving the long-term outcome of the P. magellanicus fishery under potential global change.

Funding: This study was funded by the NOAA Grant # NA12NOS4780145 ( www.noaa.gov ) and by the WestWind Foundation. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

In order to maintain a sustainable fishery into the future, it is important that all stakeholders involved in both the management and exploitation of the fishery understand possible futures of the P. magellanicus fishery and the potential impacts of decision-making. In this work, we expand on the model described in Cooley et al. [ 13 ] by incorporating different future scenarios to inform planning for long-term change. Moreover, new elements have been added to the model to include the economic development associated with different growth and emissions scenarios (the RCP pathways); economic development was previously held constant in Cooley et al. [ 13 ]. We designed a decision-support framework that explores multiple combinations of potential future scenarios to provide an ensemble of model output varying major influences on the fishery as a whole. In this manuscript, we describe a subset of those scenarios to address the following questions: how might the future trajectory of the P. magellanicus fishery change under future climate warming and ocean acidification? How do differing management regimes influence the long-term outcomes of the P. magellanicus fishery? In this work, we designed future scenarios that incorporate potential acidification impacts, future climate scenarios that affect economic development, fisheries management, and changing fuel costs (described in more detail below).

The US Atlantic sea scallop (Placopecten magellanicus) is an ideal test species to apply integrated assessment modeling to project the impacts of global change on a wild-caught fishery. The P. magellanicus fishery is one of the most valuable wild-caught fisheries in the US, regularly worth roughly $500 million (USD) in ex-vessel revenue [ 16 ]. This fishery was severely overfished in the early to mid-1990s, but was rapidly rebuilt by the early 2000s using a combination of fishing effort reductions, gear restrictions, and rotational as well as long-term fishery closures [ 17 ]. Because the P. magellanicus fishery is currently sustainable, stakeholders and managers have the opportunity to consider the impacts of long-term environmental change on the fishery stock, yield, and economic benefits.

Marine mollusks, specifically bivalves, are impacted in many ways by acidification. Their often complex, multi-stage life-cycle leads to potential bottlenecks where the chemical environment is particularly important, such as during metamorphoses from various larval stages prior to settlement [ 10 ]. Many species have shown increased larval mortality due to acidification, and larvae that survive often have deformed shell structures that suggest potential reductions in fitness during juvenile or adult stages [ 10 – 12 ]. Experimental manipulations of juvenile and adult bivalves suggest reduced growth and calcification rates under acidified conditions [ 7 , 8 , 13 ]. Further, shellfish predator-prey interactions are hypothesized to be influenced by acidification, due to decreased shell thickness and strength [ 14 ], reduced escape performance [ 15 ], and decreased behavioral responses to predators [ 14 ].

Ocean acidification, the process where increased atmospheric carbon dioxide (CO 2 ) concentration reduces ocean pH and calcium carbonate saturation state [ 1 ], has already been implicated in negative impacts on the aquaculture industry on the US West Coast [ 2 ]. Laboratory studies for a number of other economically important marine species suggest ocean acidification has the potential to significantly impact fisheries landings and revenues regionally and around the world [ 3 – 6 ]. Marine mollusks appear to be particularly sensitive to ocean acidification due to the sensitivity of the calcification process to seawater chemistry during shell building [ 6 – 8 ]. Mollusks make up approximately 22 and 15% of the wild-caught fisheries yield globally and in the US, respectively [ 9 ]; therefore, understanding sensitivities of wild-caught fisheries to ocean acidification is an important step in the long-term sustainable management of these species.

Some of our scenarios overlap in design with the results presented in Cooley et al. [ 13 ]. Similar scenarios include forcings of RCP8.5, ABC only management, larval mortality and growth rate impacts, and no fuel cost increases. However, these overlapping scenarios differ substantially in underlying socio-economic conditions because this analysis includes the economic development associated with the RCPs that were held constant in Cooley et al. [ 13 ]. For example, all four RCPs project increasing GDP, population, and PCDI ( Fig 2 ), which affect the national demand for and price of scallops.

Climate scenarios incorporate changes in fuel costs associated with carbon taxation as well as economic development used in the GCAM projections. Total fuel price is calculated as the sum of the base price, determined from the growth rate, and the carbon tax. Ocean (OA) acidification impacts include either no impact, or combinations of increasing larval mortality (Larvae), reduced growth rates (Growth), and increased mortality of small scallops due to predation (Predation). Management impacts include either no set catch limits, or combinations of maximum allowable biological catch (ABC), varying reference points due to changing growth rates (F MSY ), and closed areas (10% closure).

The set of scenarios described above generate a 4x4x4x4 hypercube of 256 possible combinations of impacts, ranging from no change of any drivers, to a high degree of climate impacts, management, and economic change ( Table 1 ). For each future scenario, the full IAM is run with stochastically varying recruitment parameters drawn from distributions determined by the underlying data (see [ 13 ]) and stochastically varying future temperatures determined from the projections shown in Fig 2 . All figures shown summarize an ensemble of 100 model runs for each scenario, and the results for each scenario are presented as the mean ± one standard deviation from the ensemble. The stochastic model runs for all scenarios yielded 25,600 individual simulations.

Fuel costs can be up to 80% of scallop boat operating costs [ 18 ]. In a scenario incorporating climate policies, future fossil fuel prices may be strongly influenced by possible carbon taxation levels. The US EIA [ 30 ] develops scenarios to predict future fuel costs under various economic and policy scenarios. The reference case assumes current policies and economic development, which projects that the nominal diesel fuel price per gallon will increase at a rate of 0.7%/yr. To estimate the impact of climate policy on fuel costs, the EIA assumes climate policies where $1 per ton carbon tax is equivalent to $0.01 per gallon diesel fuel tax ( Fig 2D ). In our scenario framework, we apply four different fuel price growth rates (1.4%, 0.7%, 0.35%, 0%) combined with carbon taxes from the GCAM model output which are required to reach the specific RCP pathway such that fuel costs are calculated as: (2) where Fuel 0 is the initial fuel cost in 2012, r i is the fuel price growth rate of the scenario i, and CarbonTax j,t is the carbon tax estimated using GCAM for climate scenario j in year t.

The major drivers of the socioeconomics of the industry are economic development, specifically per capita disposable income (PCDI, which impacts scallop pricing and demand) and fuel costs (which impacts industry operating costs and crew incomes). To develop trajectories for future socioeconomic scenarios, we used the output from the GCAM integrated assessment model which developed the RCP4.5 scenario [ 23 – 25 ]. Each official RCP scenario has been generated using a different integrated assessment model with separate underlying drivers and assumptions. In order to maintain consistency between model assumptions for the future scenarios, we used projections of economic development and carbon taxes from GCAM’s estimates of the other RCP scenarios. We converted US GDP and population projections to PCDI by correcting GDP per capita data to PCDI through a derived correlation using historical data from US Bureau of Economic Analysis of US population (pop), GDP, and PCDI data corrected to 2011 USD ( Eq 1 ): (1) where PCDI 2011 is the historical per capita disposable income corrected to 2011 USD, GDP 2011 is the historical US GDP corrected to 2011 USD, and pop is the historical population. A and B are constants derived as 0.8025 ± 0.0286 and 2383 ± 1089 (r 2 = 0.984, p < 0.0001), respectively. Future PCDI, corrected to 2011 USD, is expected to increase by a factor of 2.5–3 by the end of century under all four climate scenarios analyzed in this study ( Fig 2C ). There is considerable uncertainty in projections of energy use, emissions scenarios, and economic development that has begun to be recently explored in greater detail using the future Shared Socioeconomic Pathways (SSPs) [ 26 ]. Given that our temperature and atmospheric CO 2 projections were based upon the RCP scenarios, we chose to the use the RCP projections of GDP and population to generate our PCDI projection. The impacts of different economic development narratives could be explored in more detail using the new SSPs but would be beyond the scope of this study.

The “high” impact case is defined by other possible impact pathways beyond just growth and calcification. Recent work on mollusk species suggests that predator-prey interactions such as behavior, cue detection, or shell thickness may be altered as a result of ocean acidification [ 14 ]. Mollusk shells are the first line of defense for many species, and if shell thickness is compromised, scallops may be more susceptible to predation [ 14 ]. Early studies from Pecten maximus, a similar species of scallop found in the Northeast Atlantic, suggests that swimming behavior may be compromised due to ocean acidification, reducing the escape performance of scallops under future climate scenarios [ 15 , 21 ]. The majority of predation on juvenile P. magellanicus (20-90mm shell height) is due to Cancer spp. crabs; these scallops generally can escape sea stars (e.g., Asterias spp.) by swimming. Scallops larger than 70-90mm are currently invulnerable to Cancer predation due to their thick shells [ 22 ]. We hypothesize that ocean acidification may reduce both shell strength and swimming ability, thus reducing the scallops’ defenses against both type of predators. Because there are no empirical relationships to estimate these effects, in the “high” impact case we increase natural mortality of small scallops (< 90mm) proportionally with the change in saturation state.

Four sets of increasing biological impacts were simulated representing none, low, medium and high impacts. “No” impact is defined as maintaining constant growth rates and recruitment throughout the simulation independent of temperature and CO 2 . Although no studies to date regarding ocean acidification response have been published on P. magellanicus, from other bivalve species, we expect that adult growth or calcification rates and larval survival may be negatively impacted by rising CO 2 [ 13 ]. “Low” impacts of ocean acidification are defined as reductions in larval survival with carbonate mineral saturation state alone, while “medium” impacts are both reductions in larval survival with saturation state and decreased growth and calcification rates, as described by Cooley et al. [ 13 ] as a function of saturation anomaly.

A) Atmospheric CO 2 from the Representative Concentration Pathways (RCPs), B) change in sea surface temperature from 2000–2006 (mean ± SD) from 10 global earth system models in the 10x10 degree region containing the Mid-Atlantic Bight and Georges Bank scallop populations, C) US per-capita disposable income trajectories corrected to 2011 USD, and D) carbon tax converted to potential diesel fuel tax associated with each RCP.

Climate and biogeochemical scenarios were developed from the IPCC AR5 RCP scenarios. Major biogeochemical influences include atmospheric CO 2 and oceanic temperatures. Atmospheric CO 2 trajectories were used from the RCPs [ 19 ] ( Fig 2A ), and temperature trends were obtained from the 10 global earth system models used in Bopp et al. [ 20 ] from the CMIP5 database. The projected SST fields from RCP2.6, 4.5, 6, and 8.5 were interpolated to a 1°x1° grid consistent across all models. We quantified regional trends in area-weighted mean monthly SST fields from a 10° x 10° area containing the Georges Bank and Mid-Atlantic Bight regions in the Northwest Atlantic. We quantified anomalies from the mean temperatures of the first five years of future projections (2006–2010), and applied stochastic temperature trajectories from the projection distribution derived from the model ensemble to the biogeochemical submodel ( Fig 2B , SST).

To explore the future of the US Atlantic sea scallop industry under climate scenarios over the next century, we identified four major areas of interest: 1) potential ocean acidification impacts, 2) future climate scenarios that incorporate economic development, 3) fishery management scenarios, and 4) future fuel costs. Below, we describe the major features of each scenario.

The economic submodel is based on economic modeling of the sea scallop fishery by the New England Fisheries Management Council [ 18 ]. The submodel uses price and cost models that include terms for landings, per-capita disposable income (an indication of economic development), scallop imports and exports, fuel costs, days at sea, and number of crew members. From yearly estimated price and costs, the economic model determines the optimal number of days at sea to fish based on a rules analysis maximizing net profit and adhering to management set maximum allowable biological catch (ABC) that is determined as the catch associated with a precautionary fishing mortality (F ABC ) that is a slight reduction in the fishing mortality at maximum sustainable yield (F MSY ). The economic submodel is linked to the scallop population model through the management set limits on catch and the scallop pricing analysis, and linked to the biogeochemical model through the RCP scenarios.

The biogeochemical submodel is a two-box ocean model (surface and bottom waters) with separate sub-modules for Georges Bank and Mid-Atlantic Bight regions. Carbonate chemistry is explicitly modeled including terms for air-sea gas exchange, primary production, and calcium carbonate production in the surface box, and biological export and organic matter remineralization in the bottom water box. The two-box model also includes terms for temperature and salinity to determine seasonal changes in stratification and mixing, and the biogeochemical model parameters were trained with data from the 2000–2010 period. The biogeochemical model in the IAM is linked to the population model through temperature and calcium carbonate mineral saturation state impacts on adult growth and larval mortality. The biogeochemical model is linked to the socio-economic model through the future climate scenarios, from the IPCC Representative Concentration Pathways (RCPs), which set future atmospheric CO 2 concentration.

The scallop population submodel is a size-based matrix population model that was simplified from the sea scallop fisheries management model, the Scallop Area Management Simulator (SAMS). The SAMS model splits the scallop population into a number of distinct geographic units with individual populations and growth rates based on historical survey data. The reduced population submodel used in the IAM described in Cooley et al. [ 13 ] separates the sea scallop population into two geographic units, Georges Bank and the Mid-Atlantic Bight, and tracks each population with unique population parameters. The population submodel includes terms for recruitment, growth, maximum size, and natural, incidental, discard, and fishing mortalities, growth rates, maximum sizes, and recruitment.

Cooley et al. [ 13 ] describe an integrated assessment model (IAM) for the P. magellanicus fishery. This model combines elements of fisheries management models that include matrix population models and socio-economic models with reduced-form biogeochemical modeling to project the future fishery response to changes in environmental and economic conditions. The IAM incorporates ocean acidification and warming into fisheries projections through altered growth rates and larval survival. Based on economic viability and stock biomass, the IAM forecasts fisheries yield and economic benefits under future conditions [ 13 ]. We briefly summarize the model design below. A conceptual illustration of the IAM is given in Fig 1 .

3 Results and discussion

This study analyzes the future of the P. magellanicus fishery under the 4x4x4x4 hypercube that generates 256 possible combinations of impacts, ranging from no change of any drivers, to a high degree of climate impacts, management, and economic change, including both increases in fuel costs and GDP as well as population growth (Table 1). Of the full database, we focus this manuscript on describing the patterns in the impacts of management and ocean acidification scenarios, for RCP8.5 and RCP4.5, a business-as-usual and moderate-strength climate policy scenario, respectively.