Abstract and Figures

Several studies have documented fish populations changing in response to long-term warming. Over the past decade, sea surface temperatures in the Gulf of Maine increased faster than 99% of the global ocean. The warming, which was related to a northward shift in the Gulf Stream and to changes in the Atlantic Multidecadal Oscillation and Pacific Decadal Oscillation, led to reduced recruitment and increased mortality in the region’s Atlantic cod (Gadus morhua) stock. Failure to recognize the impact of warming on cod contributed to overfishing. Recovery of this fishery depends on sound management, but the size of the stock depends on future temperature conditions. The experience in the Gulf of Maine highlights the need to incorporate environmental factors into resource management.
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Climate change is reshaping ecosystems in ways that impact
resources and ecosystem services (1). Fisheries, with their
tight coupling between ecosystem state and economic
productivity, are a prime example of interacting social-
ecological systems. The social and ecological value of a
fishery depends first and foremost on the biomass of fish,
and fishing has often been the dominant driver of the status
of the resource and the economics of the fishing community.
Modern fisheries management is designed to reduce
harvesting levels in response to low stock biomass (and vice
versa), creating a negative feedback that, in theory, will
maintain steady long-term productivity (2).
A failure to detect changes in the environment or to act
appropriately when changes are detected can jeopardize
social-ecological systems (3). As climate change brings
conditions that are increasingly outside the envelope of past
experiences, the risks increase. The Gulf of Maine has
warmed steadily, and the record
warm conditions in 2012
impacted the fishery for
American lobster (4). Here, we
consider how ocean warming
factored into the rapid decline of
the Gulf of Maine cod stock (5).
We used sea surface
temperature data to characterize
temperature trends in the Gulf
of Maine since 1982 and over the
last decade (2004-2013). We
compared the changes in this
region with trends around the
globe and related temperature
variability to an index of Gulf
Stream position and the Pacific
Decadal Oscillation and the
Atlantic Multidecadal Oscillation.
We then examined the impact of
temperature conditions in the
Gulf of Maine on the
recruitment and survival of
Atlantic cod. The resulting
temperature-dependent population
dynamics model was used to
project the rebuilding potential
of this stock under future
temperature scenarios.
From 1982-2013, daily
satellite-derived sea surface
temperature in the Gulf of
Maine rose at a rate of 0.03°C
yr−1 (R2 = 0.12, p < 0.01, n =
11,688; Fig. 1A). This rate is
higher than the global mean rate
of 0.01°C yr−1 and led to gradual
shifts in the distribution and
abundance of fish populations (68). Beginning in 2004, the
warming rate in the Gulf of Maine increased more than
seven-fold to 0.23°C yr−1 (R2 = 0.42, p < 0.01, n = 3,653). This
period began with relatively cold conditions in 2004 and
concluded with the two warmest years in the time series.
The peak temperature in 2012 was part of a large “ocean
heat wave” in the northwest Atlantic that persisted for
nearly 18 months (4).
The recent 10 year warming trend is remarkable, even for
a highly-variable part of the ocean like the northwest
Atlantic. Over this period, substantial warming also
occurred off of western Australia, in the western Pacific, and
in the Barents Sea; and cooling was observed in the eastern
Pacific and Bering Sea (Fig. 1B). The global ocean has a total
area of 3.6 x 108 km2, yet only 3.1 x 105 km2 of the global
ocean had warming rates greater than that in the Gulf of
Maine over this time period. Thus, the Gulf of Maine has
Slow adaptation in the face of rapid
warming leads to collapse of the Gulf of
Maine cod fishery
Andrew J. Pershing,1* Michael A. Alexander,2 Christina M.
Hernandez,1† Lisa A. Kerr,1 Arnault Le Bris,1 Katherine E. Mills,1
Janet A. Nye,3 Nicholas R. Record,4 Hillary A. Scannell,1,5‡ James
D. Scott,2,6 Graham D. Sherwood,1 Andrew C. Thomas5
1Gulf of Maine Research Institute, 350 Commercial Street, Portland, ME 04101, USA. 2NOAA Earth System Research
Laboratory, Boulder, CO 80305, USA. 3School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook,
NY 11794, USA. 4Bigelow Laboratory for Ocean Sciences, 60 Bigelow Drive, East Boothbay, ME 04544, USA. 5School of
Marine Sciences, University of Maine, Orono, ME 04469, USA. 6Cooperative Institute for Research in Environmental
Sciences, University of Colorado, Boulder, CO 80309, USA.
*Corresponding author. E-mail: apershing@gmri.org
†Present address: Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
‡Present address: University of Washington School of Oceanography, Seattle, WA 98105, USA.
Several studies have documented fish populations changing in response to
long-term warming. Over the last decade, sea surface temperatures in the
Gulf of Maine increased faster than 99% of the global ocean. The warming,
which was related to a northward shift in the Gulf Stream and to changes in
the Atlantic Multidecadal and Pacific Decadal Oscillations, led to reduced
recruitment and increased mortality in the region’s Atlantic cod (
Gadus
morhua
) stock. Failure to recognize the impact of warming on cod
contributed to overfishing. Recovery of this fishery depends on sound
management, but the size of the stock depends on future temperature
conditions. The experience in the Gulf of Maine highlights the need to
incorporate environmental factors into resource management.
on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from on November 5, 2015www.sciencemag.orgDownloaded from
/ sciencemag.org/content/early/recent / 29 October 2015 / Page 2 / 10.1126/science.aac9819
warmed faster than 99.9% of the global ocean between 2004
and 2013 (Fig. 1C). Using sea surface temperatures from
1900-2013, the likelihood of any 2° by 2° segment of the
ocean exceeding this 10-year warming rate is less than 0.3%.
Based on this analysis, the Gulf of Maine experienced
decadal warming that few marine ecosystems have
encountered.
As a first step toward diagnosing the potential drivers of
the recent warming trend, we correlated the quarterly
temperatures in the Gulf of Maine with large-scale climate
indicators (table S1). An index of Gulf Stream position (9)
has the strongest and most consistent relationship with Gulf
of Maine temperatures. The correlations with the Gulf
Stream Index (GSI) are positive and significant in all
quarters, with the strongest correlation occurring in
summer (r = 0.63, p < 0.01, n = 31). The Pacific Decadal
Oscillation (PDO) (10) is negatively correlated with the Gulf
of Maine temperatures during spring (r = 0.50) and
summer (r = 0.67). Summer temperatures are also
positively correlated with the Atlantic Multidecadal
Oscillation (AMO) (11) (r = 0.48, p < 0.01, n = 31).
Building on the strong correlations with summer
temperatures, we developed multiple regression models for
summer Gulf of Maine temperatures using combinations of
the three indices (Table 1). Based on AIC score, the best
model used all three indices, and this model explained 70%
of the variance in Gulf of Maine summer temperature (R2 =
0.70, p < 0.01, AIC = 46.0, n = 31). This model was slightly
better than one using GSI and the AMO (R2 = 0.66, p < 0.01,
AIC = 48.2, n = 31). We refit each model using data from
1982-2003, and then applied the model to the 2004-2012
period. The three-index and the GSI-AMO models had
nearly identical out-of-sample performance, explaining 65%
and 64% of the variance, respectively.
A long-term poleward shift in the Gulf Stream occurred
over the 20th century and has been linked to increasing
greenhouse gasses (12). Previous studies have reported an
association between Gulf Stream position and temperatures
in the northwest Atlantic (7, 13), and an extreme northward
shift in the Gulf Stream was documented during the record
warm year of 2012 (14). Although the Gulf Stream does not
directly enter the Gulf of Maine, northward shifts in the
Gulf Stream are associated with reduced transport of cold
waters southward on the continental shelf (15, 16). The
association between Gulf of Maine temperature and the
PDO suggests an atmospheric component to the recent
trend. A detailed heat-budget calculation for the 2012 event
(17) found that the warming was due to increased heat flux
associated with anomalously warm weather in 2011-2012.
These results suggest that atmospheric teleconnections from
the Pacific, changes in the circulation in the Atlantic Ocean,
and background warming have contributed to the rapid
warming in the Gulf of Maine.
The Gulf of Maine cod stock has been chronically
overfished, prompting progressively stronger management,
including the implementation of a quota-based
management system in 2010. Despite these efforts,
including a 73% cut in quotas in 2013, spawning stock
biomass (SSB) continued to decline (Fig. 2A). The most
recent assessment found that SSB in this stock is now less
than 3,000 mt, only 4% of the spawning stock biomass that
gives the maximum sustainable yield (SSBmsy) (5). This has
prompted severe restrictions on the commercial cod fishery
and the closure of the recreational fishery.
The Gulf of Maine is near the southern limit of cod, and
previous studies have suggested that warming will lead to
lower recruitment, suboptimal growth conditions, and
reduced fishery productivity in the future (1820). Using
population estimates from the recent Gulf of Maine cod
stock assessment (5), we fit a series of stock-recruit models
with and without a temperature effect (table S2). The best
models exhibited negative relationships between age-1
recruitment and summer temperatures (table S3). Gulf of
Maine cod spawn in the winter and spring, so the link with
summer temperatures suggests a decrease in the survival of
late-stage larvae and settling juveniles. Although the
relationship with temperature is statistically robust, the
exact mechanism for this is uncertain but may include
changes in prey availability and/or predator risk. For
example, the abundance of some zooplankton taxa that are
prey for larval cod has declined in the Gulf of Maine cod
habitat (21). Warmer temperatures could cause juvenile cod
to move away from their preferred shallow habitat into
deeper water where risks of predation are higher (22).
We also looked for other signatures of temperature
within the population dynamics of cod. We found a strong
association between the mortality of age-4 fish and fall
temperatures from the current year and the second year of
life (Fig. 2B, R2 = 0.57, p < 0.01, n = 21). Age 4 represents an
energetic bottleneck for cod due to the onset of
reproduction and reduced feeding efficiency as fish
transition from benthic to pelagic prey (23). Elevated
temperatures increase metabolic costs in cod (24),
exacerbating the energetic challenges at this age. The
average weight-at-age of cod in the Gulf of Maine region has
been below the long-term mean since 2002 (25), and these
poorly conditioned fish will have a lower probability of
survival (26).
The age-4 mortality relationship improves significantly
with the addition of temperatures from the second year of
life (table S6). This suggests that a portion of the estimated
age-4 mortality reflects mortality over the juvenile period
that is not explicitly captured in the assessment.
Temperature may directly influence mortality in younger
fish through metabolic processes described above; however,
we hypothesize that predation mortality may also be higher
during warm years. Many important cod predators migrate
into the Gulf of Maine or have feeding behaviors that are
strongly seasonal. During a warm year, spring-like
conditions occur earlier in the year, and fall-like conditions
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occur later. During the 2012 heat wave, the spring warming
occurred 21 days ahead of schedule, and fall cooling was
delayed by a comparable amount (4). This change in
phenology could result in an increase in natural mortality of
44% on its own, without any increase in predator biomass
(see supplementary text).
If fishing pressure had been effectively reduced, the
population should have rebuilt more during the cool years
and then declined less rapidly during the warming period.
Instead, fishing mortality rates consistently exceeded target
levels, even though fishermen did not exceed their quotas.
The quota-setting process that is at the heart of fisheries
management is highly sensitive to the number of fish aging
into the fishery in each year. For Gulf of Maine cod, age
classes 4 and 5 dominate the biomass of the stock and the
catch (5). The temperature-mortality relationship in Fig. 2B
means that during warm years, fewer fish are available for
the fishery. Not accounting for this effect leads to quotas
that are too high. The resulting fishing mortality rate was
thus above the intended levels, contributing to overfishing
even though catches were within prescribed limits.
Socioeconomic pressures further compounded the
overfishing. In order to minimize the impact of the quota
cuts on fishing communities, the New England Fishery
Management Council elected to defer most of the cuts
indicated for 2012 and 2013 until the second half of 2013.
The socioeconomic adjustment coupled with the two
warmest years in the record led to fishing mortality rates
that were far above the levels needed to rebuild this stock.
The impact of temperature on Gulf of Maine cod
recruitment was known at the start of the warming period
(20), and stock-recruitment model fit to data up to 2003 and
incorporating temperature produces recruitment estimates
(Fig. 2A, yellow diamonds) that are similar to the
assessment time series. Ignoring the influence of
temperature produces recruitment estimates that are on
average 100% and up to 360% higher than if temperature is
included (Fig. 2A, gray squares). Based on a simple
population dynamics model that incorporates temperature,
the spawning stock biomass that produces the maximum
sustainable yield (SSBmsy) has been declining steadily since
2002 (Fig. 3) rather than remaining constant as currently
assumed. The failure to consider temperature impacts on
Gulf of Maine cod recruitment created unrealistic
expectations for how large this stock can be and how
quickly it can rebuild.
We estimated the potential for rebuilding the Gulf of
Maine cod stock under three different temperature
scenarios: a “cool” scenario that warms at a rate of 0.02°
yr−1, a “warm” scenario that warms at 0.03° yr−1, the mean
rate from climate model projections, and a “hot” scenario
that follows the 0.07°C yr−1 trend present in the summer
temperature time series. If fishing mortality is completely
eliminated, populations in the cool and warm scenarios
could rebuild to the temperature-dependent SSBmsy in 2025,
slightly longer than the 10 year rebuilding timeline
established by US law, and the hot scenario would reach its
target one year later (Fig. 3). Allowing a small amount of
fishing (F = 0.1) would delay rebuilding by three years in the
cool and warm scenarios and 8 years in the hot. Note that
estimating SSBmsy without temperature produces a
management target that may soon be unachievable. By
2030, a rebuilt fishery could produce more than 5,000 tons
yr−1 under the warm scenario, a catch rate close to the
average for the fishery for the previous decade. Under the
hot scenario, the fishery would be 1,800 tons yr−1small, but
potentially valuable. Thus, how quickly this fishery rebuilds
now depends arguably as much on temperature as it does
on fishing. Future management of Gulf of Maine cod would
benefit from a reevaluation of harvest control rules and
thorough management strategy evaluation of the
application of temperature-dependent reference points and
projections such as these.
As climate change pushes species poleward and reduces
the productivity of some stocks, resource managers will be
increasingly faced with trade-offs between the persistence of
a species or population and the economic value of a fishery.
Navigating decisions in this context requires both accurate
projections of ecosystem state and stronger guidance from
society in the form of new policies. Social-ecological systems
that depend on steady state or are slow to recognize and
adapt to environmental change are unlikely to meet their
ecological and economic goals in a rapidly changing world.
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ACKNOWLEDGMENTS
This work was supported by the NSF’s Coastal SEES Program (OCE-1325484; AP,
MA, CH, AL, KM, JN, HS, JS, and AT), the Lenfest Ocean Program (AP, AL, KM, and
GS), and institutional funds from the Gulf of Maine Research Institute (LK) and the
Bigelow Laboratory for Ocean Sciences (NR). The lead author’s knowledge of fishery
management was greatly enhanced by discussions with Patrick Sullivan, Steve Ca-
drin, Jake Kritzer, and other members of the NEFMC Scientific and Statistical Com-
mittee. Michael Palmer provided helpful comments on earlier drafts of the
manuscript and facilitated access to the recent stock assessment. The manuscript
also benefitted from helpful feedback from Jon Hare and two anonymous reviewers.
The data reported in this paper are tabulated in the supplementary materials and are
available from the referenced technical reports and from the National Climate Data
Center.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/cgi/content/full/science.aac9819/DC1
Materials and Methods
Figs. S1 to S6
Tables S1 to S5
References (2735)
9 July 2015; accepted 23 September 2015
Published online 29 October 2015
10.1126/science.aac9819
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Index, PDO = Pacific Decadal Oscillation Index, AMO = Atlantic Multidecadal Oscillation Index. The final model
uses all three indices. The first set of statistics refer to the models fit to the entire 1982-2013 record. The models
were also fit to the 1982-2003 period then projected on to the 2004-2013 period. The last two columns
summarize the out of sample performance of the models.
Time series 1 Time series 2
1982-2013
2004-2013 Out of Sample
R
2
p
AIC
r
2
p
GSI
0.39
0.00
63.92
0.50
0.00
PDO 0.58 0.00 54.41 0.54 0.00
AMO
0.66
0.00
48.15
0.64
0.00
PDO
0.45
0.00
60.77
0.28
0.01
AMO 0.50 0.00 59.78 0.32 0.01
AMO
0.23
0.01
71.06
0.11
0.13
All 0.70 0.00 45.99 0.65 0.00
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Fig. 1.
Sea surface temperature trends from the Gulf of Maine and the global ocean.
(
A
) Daily (blue, 15d smoothed)
and annual (black dots) SST anomalies from 1982-2013 with the long-term trend (black dashed line) and trend over the
last decade (2004-2013) (red solid line). (
B
) Global SST trends (° yr−1) over the period 2004-2013. The Gulf of Maine is
outlined in black. (
C
) Histogram of global 2004-2013 SST trends with the trend from the Gulf of Maine indicated at the
right extreme of distribution.
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Fig. 2. Relationships between Gulf of Maine cod and temperature. (A) Time series of Gulf of Maine cod spawning
stock biomass (blue), and age-1 recruitment (green) from the 2014 assessment. Cod age-1 recruitment modeled
using adult biomass and summer temperatures (dashed line). The gray squares are recruitment estimated using a
model without a temperature effect fit to data prior to 2004. The yellow diamonds are a temperature-dependent
model fit to this earlier period. (
B
) Mortality of age-4 cod as a function of temperature (R2 = 0.57, p < 0.01, n = 21). The
temperature is composed of the fall values from the current year and three years prior, weighted using the
coefficients from the linear model.
/ sciencemag.org/content/early/recent / 29 October 2015 / Page 8 / 10.1126/science.aac9819
Fig. 3. Temperature-dependent rebuilding potential of Gulf of Maine cod. We simulated a population
growing from the 2013 biomass (black curves) without fishing under three temperature scenarios: a cool
scenario (solid line) represented by the 10% lower bound of the CMIP-5 ensemble, a warm scenario (heavy
line) represented by the climate model ensemble mean, and a hot scenario (“+”s) with warming at the 0.07°
yr−1 rate observed in the summer in the Gulf of Maine since 1982. This population is contrasted against an
estimate of the temperature-dependent SSBmsy (blue lines and shading), an estimate of SSBmsy without
accounting for temperature (grey dashed line), and the carrying capacity of the population (green lines and
shading). The yellow circles mark where the rebuilding population reaches the temperature-dependent
SSBmsy, squares denote when a population fished at F = 0.1 would be rebuilt.
... Globally, warming oceans have received increased attention with respect to the occurrence and intensification of HABs as water temperatures reach values that support maximum growth of these species, including A. catenella (Gobler et al., 2017;Seto et al., 2019). The Gulf of Maine is subject to global climate change and is experiencing a dramatic increase in its surface temperature regime and shift in seasonal SST phenology (Pershing et al., 2015;Thomas et al., 2017). Phenological shifts in the physical environment (e.g. ...
... The northeast North American continental shelf, including the Gulf of Maine, is among the most rapidly warming pieces of ocean on the planet (e.g. Forsyth et al., 2015;Pershing et al., 2015;Kavanaugh et al., 2017;Thomas et al., 2017). Associated with this warming is a shift in thermal phenology, with spring arriving earlier, fall later, and summer lasting longer (Thomas et al., 2017). ...
... The systematic reduction in the timing of both thermal habitats (EDTHab and BITHab) over the study period is consistent with climate-linked warming trends for the Gulf of Maine (e.g. Pershing et al., 2015;Thomas et al., 2017;Alexander et al., 2018;Balch et al., 2022). Increased temperatures, especially during summer, drive thermal phenological shifts, including earlier arrival dates of specific temperature thresholds and an average reduction in summer start date by approximately 1 day year -1 (Thomas et al., 2017). ...
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... The fate of many species across the planet are inexplicably linked with climate change. An ecosystem of particular interest is that of the Gulf of Maine, where the warming rates here are higher than most anywhere else in the oceans (Mills et al. 2013;Pershing et al. 2015). ...
... However, in recent history, the waters in this system have been warming at an alarming rate (Mills et al. 2013;Pershing et al. 2015), due in part by melting Arctic sea ice (Saba et al. 2016). This melting phenomenon is releasing a lot of fresh water into the Arctic Ocean. ...
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... marine areas in the world (Pershing et al., 2015). Rising temperatures have increased the area's susceptibility to novel and ongoing biological invasions, including that of the Asian shore crab (Hemigrapsus sanguineus). ...
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... The need to more deeply understand metabolic adaptations associated with limb loss-and other metabolic adaptations-is especially pressing considering the rapid warming in the Gulf of Maine (Pershing et al., 2015). Metabolic injury resilience and other energetic traits may be altered by rising temperatures and elevated metabolic rates associated with climate change (Parry, 1983). ...
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The Gulf of Maine (GOM) has seen an increasing number of introduced species, some of which have significantly impacted benthic community structure. In 2017, a number of specimens of the European dorid nudibranch, Doris pseudoargus, were observed on rocky ledges in waters off Cape Ann, Massachusetts. The presence of numerous specimens and egg masses suggested the species had been established before 2017. Additional field observations and literature searches revealed specimens occurring from Nova Scotia to the northern end of the Cape Cod Canal, which poses the question, when and where did the initial introduction take place and how? Genetic analysis confirmed the species as Doris pseudoargus with genomic similarities to specimens from Northern Europe. Until this introduction, the GOM had only one species of sponge feeding nudibranch, Cadlina laevis, which is a trophic specialist on one genus of sponge. Unlike this endemic, stenotrophic feeding dorid, the introduction of another large sized, sponge predator known to feed on diverse sponge species, that occur from the intertidal to at least 25 m in depth has the potential to significantly impact community structure over a wide variety of hard bottom habitats.
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