Climate vulnerability and resilience in the most valuable North American fishery
Arnault Le Brisa, Katherine E. Mills, Richard A. Wahle, Yong Chen, Michael A. Alexander, Andrew J. Allyn, Justin G. Schuetz, James D. Scott, and Andrew J. Pershing
*Gulf of Maine Research Institute, Portland, ME 04101; School of Marine Sciences, University of Maine, Orono, ME 04469; National Oceanic and Atmospheric Administration, Earth System Research Laboratory, Boulder, CO 80305; and Cooperative Institute for Research in Environmental Sciences,
University of Colorado, Boulder, CO 80309
Edited by Bonnie J. McCay, Rutgers, The State University of New Jersey, New Brunswick, NJ, and approved December 20, 2017 (received for review June 20, 2017)
Managing natural resources in an era of increasing climate impacts
requires accounting for the synergistic effects of climate, ecosystem
changes, and harvesting on resource productivity. Coincident with
recent exceptional warming of the northwest Atlantic Ocean and
removal of large predatory fish, the American lobster has become
the most valuable fishery resource in North America. Using a model
that links ocean temperature, predator density, and fishing to
population productivity, we show that harvester-driven conservation
efforts to protect large lobsters prepared the Gulf of Maine lobster
fishery to capitalize on favorable ecosystem conditions, resulting in
the record-breaking landings recently observed in the region. In
contrast, in the warmer southern New England region, the absence
of similar conservation efforts precipitated warming-induced recruitment
failure that led to the collapse of the fishery. Population projections
under expected warming suggest that the American lobster
fishery is vulnerable to future temperature increases, but continued
efforts to preserve the stock’s reproductive potential can dampen
the negative impacts of warming. This study demonstrates that,
even though global climate change is severely impacting marine
ecosystems, widely adopted, proactive conservation measures can
increase the resilience of commercial fisheries to climate change.
climate impacts | resilience | harvest strategies | population dynamics |
American lobster
Ensuring that fisheries are sustainable and resilient to increasing
climate impacts is one of the extraordinary
challenges facing marine ecosystems and coastal communities
worldwide. Current climatic trends reflecting accumulation of
greenhouse gas emissions over the past decades are already
impacting global fisheries and societies that depend on them (1–3),
and efforts to reduce emissions may not be effective before another
several decades (4). It is thus necessary to identify immediate solutions
to build resilience and adapt to expected changes. Such proactive
management requires a detailed understanding of how
environmental change and management policies interact, and quantitative
projections based on this understanding (5). The complexity of
the biophysical and socioeconomical mechanisms at play (6) and
potential synergistic effects of environmental change and management
policies (7, 8) pose a challenge for developing these projections.
In this study, we use a model that links ocean temperature,
predator density, and fishing to population dynamics to evaluate the
role of warming and harvest strategies in the simultaneous collapse
of the American lobster (Homarus americanus) fishery in southern
New England (SNE) and record-breaking landings in the Gulf of
Maine (GoM). Mechanisms that explained recent population
trajectories are then used in projections to identify harvest strategies
that promote resilience of climate-vulnerable fisheries.
The fishery for American lobster is the most valuable fishery in
both the United States and Canada, with a combined landed
value of more than $US 1.5 billion in 2015 (9, 10). The overall
increase in lobster abundance belies different trajectories within
the range of the species. The fishery in the GoM, near the center
of the species’ range, has increased dramatically, while the fishery
at the warmer southern edge in SNE has effectively collapsed (11).
The exceptional warming rate in the northwest Atlantic, well
above the global average (12), may have contributed to these divergent
trajectories (13) (Fig. 1). Warming waters have been associated
with decreased juvenile habitat (14, 15) and increased
prevalence of epizootic shell disease (16) in the southern region,
and with expanded juvenile habitat in the north (17, 18). These
environmental changes have been accompanied by the decline of
large-bodied predators in the GoM, which may have added to the
regional differences in population trajectories (17, 19).
The two regions also differ in their approach to fisheries
management. Coastal communities in Maine, where 83% of US
lobster landings occurred in 2015, have a high economic reliance
on lobster that has grown in concert with lobster abundance and
with declines in other fisheries (20). While the high reliance on
this one fishery creates socioeconomic risk in a changing climate,
it has encouraged a strong conservation ethos among the 3,500+
active owner−operators in the fishery. The fishery is divided into
local lobster zones (∼1,000 km2) with comanagement authority,
and, within these zones, harvesters have informal individual and
community fishing territories (21). Instead of quota management,
an approach that is often considered the state of the art in fishery
management, the lobster fishery is managed through a series of
fishing effort controls and size limitations. These include minimum
Significance
Climate change is impacting global fisheries and societies that
depend on them. Identifying climate adaptation measures requires
understanding how environmental changes and management
policies interact in driving fishery productivity. Coincident
with the recent exceptional warming of the northwest Atlantic
Ocean, the American lobster has become the most valuable
fishery resource in North America. Here we show that interactions
between warming waters, ecosystem changes, and differences
in conservation efforts led to the simultaneous collapse
of lobster fishery in southern New England and record-breaking
landings in the Gulf of Maine. Our results demonstrate that
sound, widely adopted fishery conservation measures based on
fundamental biological principles can help capitalize on gains
and mitigate losses caused by global climate change.
Author contributions: A.L.B. and A.J.P. designed research; A.L.B. performed research;
A.L.B., M.A.A., and J.D.S. contributed new reagents/analytic tools; A.L.B. analyzed data;
and A.L.B., K.E.M., R.A.W., Y.C., M.A.A., A.J.A., J.G.S., J.D.S., and A.J.P. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Published under the PNAS license.
1Present address: Centre for Fisheries Ecosystems Research, Fisheries and Marine Institute
of Memorial University of Newfoundland, St. John’s, NL, Canada A1C 5R3.
2To whom correspondence should be addressed. Email: arnault.lebris@mi.mun.ca.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1711122115/-/DCSupplemental.
www.pnas.org/cgi/doi/10.1073/pnas.1711122115 PNAS Early Edition | 1 of 6
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landing sizes and harvester-driven initiatives to discard lobsters
above a certain size and to protect reproductive females using a
process called “v-notching” (harvesters clip a V-shaped mark into
the tails of egg-bearing females, offering protection from harvest as
landing V-notched lobsters is prohibited). Although minimum legal
sizes have been imposed in the south, preservation of large
reproductive lobsters was not championed, creating a natural experiment
to understand the relative impact of environmental
change and harvest strategies on an important commercial species.
We developed a model that integrates multiple effects of ocean
temperature, predator density, and fishing on lobster population
dynamics. A key goal of our approach was to develop a single
model that can explain lobster population dynamics across a range
of habitats. The components of the model were developed sequentially
using life history, macroecology, and population dynamics
theories. We first quantified the life history trade-offs between
accelerated growth, earlier maturation, and reduced fecundity of
smaller-bodied adults that typically occur when ectotherms are exposed
to warmer conditions or under strong size-selective harvesting.
Second, we developed a function that synthesizes the impact of
temperature and fishing on the size spectrum of lobster predators.
Under warm conditions, the abundance of smaller-bodied lobster
predators increases, while increased fishing pressure selectively
removes larger individuals from the assemblage of predatory fishes.
Finally, we linked the recruitment of age-1 lobsters to the estimated
egg production based on the abundance and size of adults. The
function incorporates a quadratic temperature term to allow for
an optimal summer temperature for lobster recruitment (17). The
complete lobster population model was validated by comparing
hindcasted abundance with abundance estimates from the most
recent stock assessment (11).
Results and Discussion
When forced with observed monthly landings and water temperatures,
the model captures the past dynamics of both theGoM (r2 =
0.75) and SNE lobster stocks (r2 = 0.81, Fig. 2). Model-estimated
mean abundance increased by 515% from 1985 to 2014 for the
GoM stock, and decreased by 78% from 1997 to 2014 for the SNE
stock. However, when temperatures were fixed at the 1984–
1999 average, variations in abundances were much smaller for both
stocks (Fig. 2 A and B). This suggests that recent rapid warming in
the northwest Atlantic has played an integral role in driving the
boom in the American lobster fishery in the GoM and its collapse
in the warmer SNE region.
Temperature effects on recruitment (number of 1-y-old lobsters)
was the primary factor driving population abundance. Increased
individual growth rate and reduced size at maturity (22) led to an
increase in egg production in the GoM stock, but to a modest
increase in recruitment (Fig. 2C). However, the production of
1-y-old lobsters per egg was greatly enhanced by the northeastward
shift of the estimated 16.4 °C optimal summer temperature
(Fig. 3), boosting GoM stock abundance in recent years, and
explaining the northeast shift in lobster distribution (23) and the
current record high landings in Atlantic Canada (10). In contrast,
summer inshore temperatures in the south increasingly exceeded
the thermal optimum for lobster recruitment (Fig. 3), resulting in
recruitment failure in the SNE stock (15).
Differences in predation pressure and prevalence of shell
disease also contributed to the disparate population trajectories.
Fishing of large predators, including Atlantic cod, reduced predation
mortality on lobsters, precipitating the rise of lobster
abundance in the GoM (Fig. 2C). We estimated that, without the
removal of large predators, lobster abundance in the GoM would
have increased by 434% instead of 515% since 1985. In SNE, the
more diverse communities of small predators maintained an elevated
predation mortality on smaller lobsters, canceling out the
reduction of predation mortality caused by the removal of larger
predators (Fig. 2D). In contrast, the outbreak of shell disease in
1998 increased the natural mortality in SNE, contributing to the
stock collapse in the region (Fig. 2D).
Preserving larger, more fecund females is an ongoing issue in
fisheries management, and differences in the level of protection
afforded to large lobsters in the two regions amplified the effects of
ecosystem changes. In 1917, lobster harvesters in Maine began a
V-notching program to preserve reproductive females, and
V-notching of all egg-bearing females has since been mandatory.
In the 1930s, harvesters and legislators in Maine collectively
decided to impose a maximum size limit of 128 mm carapace
length (CL). In contrast, in SNE, a maximum size limit varying
from 133 mm to 171 mm CL among areas was imposed only in
2008, and the practice of V-notching is voluntary and less common.
We evaluated the role of these conservation measures on past stock
dynamics by applying the management measures from one stock to
the other. Model simulations revealed that, without conservation
measures to protect large lobsters and reproductive females, lobster
abundance in the GoM would have increased by 242% instead of
515% (Fig. 2A). On the other hand, if more restrictive conservation
measures had been implemented earlier in SNE, the stock
abundance would have decreased by only 57% instead of 78% (Fig.
2B). Our results suggest that, because of their higher fecundity, preserving
large females can dampen the negative effects and amplify the
benefits of warming.
We used the model to project trends in American lobster fisheries
out to 2050 using temperature conditions from the ensemble
of climate projections of the Climate Model Intercomparison
Project Phase 5 (CMIP5) under representative concentration
pathway (RCP) 8.5. Using constant exploitation rates equal to
the average of the last 5 y, model projections indicate that the GoM
lobster fishery is vulnerable to future temperature increases (Fig. 4A).
The warmest temperature scenario that we explored (∼0.05 °C·y−1)
gives the largest and steepest decline in abundance (−62% relative to
2014; Fig. 4A), while the coolest scenario (∼0.03 °C·y−1) shows a
more gradual decline (−40%relative to 2014; Fig. 4A). The projected
decline in abundance is caused by temperature-induced decreases in
recruitment and increases in predation mortality on small lobsters.
Model projections also showed that maintaining measures to preserve
large reproductive females can mitigate negative impacts of warming
on the GoM lobster fishery in future decades (Fig. 4B). However, an
outbreak of shell disease would amplify the temperature-induced
decreases in abundance. Model projections for the southern stock
showed that no recovery to the abundance levels observed in the mid-
1990s can be expected. A slight recovery to the mid-1980s levels is
possible if temperature follows the coolest scenario (Fig. 4C) or if
shell disease were to disappear (Fig. 4D).
-1
0
1
2
0
200
400
600
-1
0
1
2
SST anomaly (°C)
0
100
200
300
Landing proportion relative to 1984 (%)
1985 1990 1995 2000 2005 2010 2015
A
B
Fig. 1. Trends in SST anomalies (blue lines) from 1984 to 2014 and landings
(orange lines) of American lobster. (A) GoM. (B) SNE.
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Model assumptions and limitations in climate forecasts call for
caution when interpreting projections of absolute abundances.
First, the relatively coarse resolution of climate models limits the
ability to predict the frequency and strength of processes affecting
recruitment, such as marine heat waves, storms, and variation in
coastal currents (24). Recent high-resolution climate projections
show that the northwest Atlantic should warm at 3 times the global
average rate (25). This result suggests that the warmest scenario
used in this study may be more realistic. Second, we assumed that
current stock boundaries reflect actual population units with independent
demography. This assumption was necessary given the
limited understanding of American lobster population structure.
While previous studies have suggested connectivity between management
units, including the potential for upstream regions on the
Canadian shelf to contribute larvae to the GoM region (26), recruitment
mostly originates from local sources within the stock
area (27). Third, our model does not consider the potential for
rapid evolutionary adaptation (28), which could help the species
counter stressful temperature conditions. Finally, our model assumes
that temperature is the sole climatic driver of population
changes. Other stressors of climate change, such as acidification
and deoxygenation, are affecting marine ecosystems (29) and may
impact lobster productivity in the future.
There is a growing appreciation for how protecting large individuals
can increase population resilience to elevated exploitation
rates (30) and reduce fluctuations caused by climate variability (31).
The northern cod population in Atlantic Canada experienced
truncation of its age structure by selective fishing (32), which impeded
its resilience to several years of combined high exploitation
rates and poor environmental conditions and precipitated its collapse.
Similarly, the disproportionate removal of larger individuals
of five fish species in the Barents Sea increased populations’ sensitivity
to environmental fluctuations, because population growth
rates became more dependent on recruitment than on adult survival
(33, 34). Consistent with these results, the lack of conservation
measures to preserve large lobsters in SNE, combined with higher
mortality rates caused by an outbreak of epizootic shell disease,
precipitated the recruitment failure caused by rapid warming. In
contrast, the maintenance of a high egg production in the GoM
prepared the fishery to capitalize on favorable ecosystem conditions
(i.e., lower predation mortality and optimal temperature). These
results demonstrate that sound harvest strategies based on fundamental
biological principles can dampen negative and reinforce
positive effects of ecosystem changes.
The development of current harvest strategies in Maine was
facilitated by the flexibility of Maine’s Lobster Management 0
200 400 600
1985 1990 1995 2000 2005 2010 2015
0 40 80 120
Abundance (million of individuals)
0 40 80 120 0 200 400 600
Baseline Temperature Harv. Stra. Growth-Mat. Predation Shell Disease
A C
B D
Fig. 2. Hindcast of abundance of American lobster across multiple scenarios. (A and B) Estimated abundance from 1985 to 2014 for the (A) GoM and (B) SNE
stocks. Dots indicate abundance estimates from the last stock assessment (15). The blue lines show model hindcast with observed temperatures and actual
harvest strategies. Yellow lines show model hindcast with constant temperature set at the average of the 1984–1999 time period. Red lines show model
hindcast with observed temperatures but switched harvest strategies (maximum size limits and V-notching) between the two stocks. Colored areas show 95%
confidence intervals. (C and D) Estimated abundance in 2014 for (C) GoM and (D) SNE stocks. Baseline, Temperature, and Harv. Stra. (harvest strategies)
correspond to the blue, yellow, and red lines, respectively, on A and B. Growth-Mat. corresponds to a scenario in which we assumed that growth and maturity
were kept constant. Predation corresponds to a scenario in which we assumed no removal of predators by fishing. Shell Disease corresponds to a scenario that
assumed no shell disease in SNE. Error bars show 95% confidence intervals.
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Zone Law, and by the ability of industry leaders to influence legislation
(35). The informal establishment of territorial use rights
promoted a strong conservation ethos in the industry, encouraging
the adoption of sustainable harvest strategies to the detriment of
immediate economic returns. The case study of the American lobster
confirms that a strong sense of resource stewardship and flexible
governance facilitate the adoption of effective conservation measures
and confer resilience in fisheries. However, at the fishing
community level, continued reliance on one successful fishery may
present a risk (20), especially given that rates of ecosystem changes
can outpace reactive management decision processes (12). Coastal
communities should adopt anticipatory adaptation measures, such
as diversifying their portfolios of economic opportunities (36), to
build resilience against the multiple impacts of climate change.
Materials and Methods
Population Dynamics Model. The dynamics of lobster populations from the GoM
and SNE were reconstructed using a temperature-dependent size-based model
(Fig. S1). The number of lobsters at size was simulated using a cohort equation,
Ns,x, y,t+1 =Ns,x,y,t e−Ms,x,y=12 +Rs,x,y,t −Cs,x,y,t , [1]
where Ns,x,y,t is the number of lobsters of stock s in size bin x (43 size bins
from 13 mm to 223 mm CL) in year y and month t, Cs,x,y,t is the number of
lobsters landed, Ms,x,y is the instantaneous rate of natural mortality, and
Rs,x,y,t is the number of recruits. Individual growth was modeled using a
temperature-dependent von Bertalanffy growth function (see SI Materials
and Methods).
The instantaneous rate of natural mortality was modeled with three
components: a predation mortality (Mp), a background mortality (Mo), and a
disease mortality (Md). The disease mortality was imposed only for SNE
starting in 1998 following the outbreak of the epizootic shell disease that
occurred in the region (11, 16). Because of the limited information of the
effect of shell disease, we set Md =0.1 for all size classes (11). The background
mortality ensured that nonpredated large lobsters experienced mortality and
was assumed to be a function of asymptotic mass (37), Mos,y =τm−λ
∞ s,y. The
predation mortality built upon previous work on community size spectrum
(38, 39). Predation mortality for a lobster of mass m was assumed to be
proportional to the density of predators Npðmp, s, yÞ in mass bin mp, for stock
s and year y, to the probability of being ingested during an encounter with a
predator φðmp,mÞ, and to the volume search by an individual predator VðmpÞ,
Mpðm, s, yÞ=
mZp max
mp min
Np
mp, s, y
φ
mp,m
V
mp
dmp. [2]
The volume search by a predator was assumed to be an allometric function of
mass (40) VðmpÞ=θmωp
. The probability of ingestion was modeled using a
function similar to a log-normal density function (41),
Fig. 3. Spatial recruitment index. Recruitment was estimated using a Ricker model based on TEP and a quadratic SST term. On this figure, recruitment was
normalized across years and across the spatial domain.
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φ
mp,m
=exp
−ln
m
ρ mp
2σ2
, [3]
where ρ is the preferred predator−prey size ratio, and σ is the width of the
function (Table S1); φðmp,mÞ takes a value of 1 at ρ. Finally, the density of
predators was modeled with a linear size spectrum,
log
Np
mp, r, y
=μðr, yÞ+log
mp
* ϑðr, yÞ. [4]
The size spectrum of lobster predators was compiled based on abundance
data from scientific bottom-trawl surveys. Parameters μ and ϑ were regionspecific
and varied annually due to the effects of temperature and fishing on
the size spectrum (see SI Materials and Methods).
Following evidence of cannibalism in the species (42), we used a Rickermodel
to estimate recruit numbers from total egg production (TEP) (see SI Materials
and Methods). We extended the Ricker model with a quadratic temperature
term to consider thermal optimum for lobster settlement (43). The model was
fitted to both the GoM and SNE stock combined using a mixed-effects model,
allowing for stock specific productivities but a common temperature effect,
Rs,y =αs TEPβsTEPs,y−1
s,y−1 eγSSTy eδSST2
y «s,y , [5]
where Rs,y is the number of recruits for stock s at year y, SSTy is the summer
inshore sea surface temperature (SST) from the year of settlement, αs and βs
are random effect coefficients specific to each stock, γ and δ are fixed effect
coefficients common to both stocks, and «s,y is a log-normal error. Recruitment
occurred in July (66%) and October (34%), and recruits were
distributed to the first three size classes with the following proportions:
0.658, 0.334, and 0.008 (44). This stock recruitment (SR) function assumed
that the two stocks correspond to closed populations: No dispersal of eggs or
exchange of recruits occurs between the two populations and with other
lobster populations.
Model Simulations. We evaluated the model’s capacity to reconstruct past
dynamics for the GoM and SNE lobster stocks by comparing our abundance
estimates with abundance estimates from the last stock assessment report
(11). Model uncertainty was quantified by a bootstrap of the residuals of the
predator size spectrum, maturity, and SR functions (1,000 iterations). We
also considered the uncertainty arising from averaging temperature data
and projections across the spatial domains by sampling temperature from a
normal distribution of mean and SD estimated using all of the temperature
cells that composed each spatial domain (see SI Materials and Methods).
Using different hindcast simulation scenarios, we evaluated the role of five
factors that may have contributed to the simultaneous collapse of the lobster
fishery in SNE and record landings in the GoM. The “baseline” simulation used
observed temperatures and actual harvest strategies. The “temperature”
simulation used constant temperatures equal to the mean of the first half of
the time series (1984–1999) to evaluate the role of the recent rapid warming
in the northeast United States. The “harvest strategies” simulation evaluated
the role of the difference in harvest strategies by swapping management
strategies between the two regions. V-notching and a maximum size limit of
128 mm CL were imposed in SNE starting in 1996, while no V-notching and a
maximum size limit of 140 mm CL were imposed in the GoM throughout the
time series. In the “growth and maturity” simulation, growth rate and size at
maturity were set constant and equal to values observed in 1984. In the
“predation” simulation, we removed temporal trends in the lobster predator
size spectrum to evaluate the role of the fishing of predators in lobster
abundance. Finally, in the “shell disease” simulation, we removed the natural
mortality effects caused by shell disease in SNE.
Lastly, we performed five model projections out to 2050 to evaluate future
impacts of warming, changes in harvest strategies, and shell disease prevalence
on population abundance. The first three projections used the mean,
5th percentile, and 95th percentile of the ensemble of climate projections of
CMIP5 (see SI Materials and Methods). Projections from only RCP 8.5 were
used to limit the number of simulations, and because projections of the
radiative forcing are similar across the RCPs out to ∼2050 (45). Exploitation
1990 2000 2010 2020 2030 2040 2050
0 40 80 120 0 200 400 600
Abundance (million of individuals)
Baseline Harv. Stra. Shell Disease
A
B
C
D
0 40 80 120 0 200 400 600
Fig. 4. Projections of American lobster abundance. (A and B) Estimated abundance from 1985 to 2050 for the (A) GoM and (B) SNE stocks. Projections use the
mean (solid lines), the 5th percentile (dashed lines), and the 95th percentile (dotted lines) of temperature projections from the CMIP5 ensemble of climate
projections using RCP 8.5. Colored areas show 95% confidence intervals. (C and D) Estimated abundance in 2050 for (C) GoM and (D) SNE stocks using mean
temperature projections but alternative harvest strategies and shell disease. Baseline corresponds to solid lines on A and B. Harv. Stra. tests the effects of
inverting maximum size limits and participation in V-notching between the stocks. Shell Disease tests the effects of inverting shell disease prevalence between
the stocks. Error bars show 95% confidence intervals.
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rates were set constant and equal to the average of the last 5 y (2010–2014).
The harvest strategies observed in 2014 were used. In the fourth simulation,
we switched harvest strategies between the two stocks, similar to the
hindcast “harvest strategies” simulation. V-notching was applied to SNE
instead of GoM, and maximum fishing sizes of 140 mm CL and of 128 mm CL
were applied to the GoM and SNE stocks, respectively. In the fifth simulation,
we removed the shell disease mortality from the SNE stock and applied
it to the GoM stock. The fourth and fifth simulations used the mean of the
ensemble of climate projections and the 2010–2014 average exploitation
rates. In the five model projections, predator density was modeled as a function
of projected temperature and fishing pressure using the same linear size spectrum
function as in the model hindcast (Eq. 2).
ACKNOWLEDGMENTS. The authors thank Burton Shank, Carl Wilson, Curt
Brown, and Andy Thomas, for helpful discussions; and Mike Fogarty and Jon
Hare for their comments. This work was supported by the National Science
Foundation’s Coastal SEES Program Grant OCE-1325484 (to A.L.B., A.J.P.,
K.E.M., Y.C., R.A.W., M.A.A., and J.D.S.).
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