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Rapid Global Expansion of Invertebrate Fisheries: Trends, Drivers, and Ecosystem Effects

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Worldwide, finfish fisheries are receiving increasing assessment and regulation, slowly leading to more sustainable exploitation and rebuilding. In their wake, invertebrate fisheries are rapidly expanding with little scientific scrutiny despite increasing socio-economic importance. We provide the first global evaluation of the trends, drivers, and population and ecosystem consequences of invertebrate fisheries based on a global catch database in combination with taxa-specific reviews. We also develop new methodologies to quantify temporal and spatial trends in resource status and fishery development. Since 1950, global invertebrate catches have increased 6-fold with 1.5 times more countries fishing and double the taxa reported. By 2004, 34% of invertebrate fisheries were over-exploited, collapsed, or closed. New fisheries have developed increasingly rapidly, with a decrease of 6 years (3 years) in time to peak from the 1950s to 1990s. Moreover, some fisheries have expanded further and further away from their driving market, encompassing a global fishery by the 1990s. 71% of taxa (53% of catches) are harvested with habitat-destructive gear, and many provide important ecosystem functions including habitat, filtration, and grazing. Our findings suggest that invertebrate species, which form an important component of the basis of marine food webs, are increasingly exploited with limited stock and ecosystem-impact assessments, and enhanced management attention is needed to avoid negative consequences for ocean ecosystems and human well-being.
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Rapid Global Expansion of Invertebrate Fisheries: Trends,
Drivers, and Ecosystem Effects
Sean C. Anderson
1
*, Joanna Mills Flemming
2
, Reg Watson
3
, Heike K. Lotze
1
1Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada, 2Department of Mathematics and Statistics, Dalhousie University, Halifax, Nova Scotia,
Canada, 3Fisheries Centre, University of British Columbia, Vancouver, British Columbia, Canada
Abstract
Background:
Worldwide, finfish fisheries are receiving increasing assessment and regulation, slowly leading to more
sustainable exploitation and rebuilding. In their wake, invertebrate fisheries are rapidly expanding with little scientific
scrutiny despite increasing socio-economic importance.
Methods and Findings:
We provide the first global evaluation of the trends, drivers, and population and ecosystem
consequences of invertebrate fisheries based on a global catch database in combination with taxa-specific reviews. We also
develop new methodologies to quantify temporal and spatial trends in resource status and fishery development. Since
1950, global invertebrate catches have increased 6-fold with 1.5 times more countries fishing and double the taxa reported.
By 2004, 34% of invertebrate fisheries were over-exploited, collapsed, or closed. New fisheries have developed increasingly
rapidly, with a decrease of 6 years (+3 years) in time to peak from the 1950s to 1990s. Moreover, some fisheries have
expanded further and further away from their driving market, encompassing a global fishery by the 1990s. 71% of taxa (53%
of catches) are harvested with habitat-destructive gear, and many provide important ecosystem functions including habitat,
filtration, and grazing.
Conclusions:
Our findings suggest that invertebrate species, which form an important component of the basis of marine
food webs, are increasingly exploited with limited stock and ecosystem-impact assessments, and enhanced management
attention is needed to avoid negative consequences for ocean ecosystems and human well-being.
Citation: Anderson SC, Mills Flemming J, Watson R, Lotze HK (2011) Rapid Global Expansion of Invertebrate Fisheries: Trends, Drivers, and Ecosystem Effects. PLoS
ONE 6(3): e14735. doi:10.1371/journal.pone.0014735
Editor: Steven J. Bograd, National Oceanic and Atmospheric Administration/National Marine Fisheries Service/Southwest Fisheries Science Center, United States
of America
Received March 11, 2010; Accepted January 17, 2011; Published March 8, 2011
Copyright: ß2011 Anderson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Financial support is acknowledged from the Natural Sciences and Engineering Research Council of Canada with grants to HKL and JMF; the Sloan
Foundation (Census of Marine Life, Future of Marine Animal Populations) with grants to HKL; and the Sea Around Us Project, a scientific collaboration between the
University of British Columbia and the Pew Environment Group. This project was part of a National Center for Ecological Analysis and Synthesis working group
funded by the National Science Foundation and the Gordon and Betty Moore Foundation. The funders had no role in study design, data collection and analysis,
decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: sean.anderson@dal.ca
Introduction
Global finfish catches from capture fisheries peaked in the 1980s
and have declined or remained stable since the early 1990s, yet
global invertebrate catches have continued to climb [1]. Although
some invertebrate fisheries have existed for centuries [2–4], many
others have commenced or rapidly expanded over the past 2–3
decades [5,6]. Today, shrimp has the largest share of the total
value of internationally-traded fishery products (17% in 2006,
including aquaculture), followed by salmon (11%), groundfish
(10%), tuna (8%), and cephalopods (4%) [1]. In several ways,
invertebrate fisheries represent a new frontier in marine fisheries:
they provide an alternative source of animal protein for people, job
opportunities in harvesting and processing, and substantial
economic opportunities for communities due to their high value
and expanding markets [1,5,6]. Yet, while finfish fisheries [7] and
some more established invertebrate fisheries [8–11] have received
increasing assessment, regulation, and rebuilding, many inverte-
brate fisheries do not get the same level of attention or care. They
are typically not assessed, not monitored, and often unregulated
[1,2,5,6,12], which threatens their sustainable development
despite their increasing social, economic, and high ecological
importance [6,13].
The increase in invertebrate fisheries is in part a response to
declining finfish catches that caused many fishermen to switch to
new target species, often further down the food web [6,14]
although in many regions lower-trophic-level fisheries were added
without declines in higher-trophic-level fisheries [15]. At the same
time, the abundance and availability of many invertebrates may
have increased due to release from formerly abundant finfish
predators [16]. Once thought to be particularly resistant to over-
exploitation [17], an increasing number of historical [3,4] and
recent invertebrate fisheries [2,5,12] tell a different story. Thus, in
light of their increasing importance, we evaluated the current
status, as well as the spatial and temporal trends of invertebrate
fisheries around the world. Further, we aimed to assess their
underlying drivers, and population and ecosystem consequences.
Unfortunately, stock assessments and research survey data that
are available to evaluate many finfish populations [7] are often
lacking for invertebrates [6,12,13]. Therefore, we used the Sea
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Around Us Project’s catch database (Text S1) as the best available
data source to analyze temporal and spatial trends in invertebrate
fisheries on a global scale. It consists largely of a quality-checked
version of the Food and Agriculture Organization’s (FAO) catch
database supplemented by regional and reconstructed datasets
covering 302 invertebrate species or species groups (taxa) over 175
countries from 1950–2004 [18]. Wherever possible we have
corroborated the observed patterns with recent taxa-specific global
reviews (Text S1).
Results and Discussion
Since 1950, invertebrate fisheries have rapidly expanded on
multiple scales, and today operate around the world (Fig. 1A). In
2000–2004, the highest concentrations of catch per unit area by
Large Marine Ecosystem (LME) were in the Yellow Sea, East
China Sea, and the Northeast U.S. Continental Shelf, followed by
the Newfoundland-Labrador Shelf, South China Sea, and
Patagonian Shelf. The bulk of the catch in these areas consisted
of bivalves, shrimps, squids, and crabs (Table S1). Catches for all 4
of the larger invertebrate taxonomic groups (crustaceans, bivalves,
cephalopods, and echinoderms) were heavily concentrated in the
Yellow Sea and East China Sea (Fig. S1). In addition, catches for
crustaceans were highly concentrated off the Newfoundland-
Labrador Shelf, bivalves on the Northeast U.S. Continental Shelf,
cephalopods off the Patagonian Shelf, and echinoderms off the
Humboldt Current (Fig. S1). Since 1950, the total reported catch
of invertebrates has steadily increased 6-fold from 2 to 12 million t
(Fig. 1B). In comparison, the catch of invertebrates and finfish
combined increased 5-fold over the same period, beginning to
decline in the late 1980s [14,19]. The increase in invertebrate
catch is not driven by only a few countries, as the average catch
per country has more than doubled (Fig. 1B). Also, in 2004 there
were 1.5 times more countries fishing for twice as many
invertebrate taxa compared to 1950 (Fig. 1C). This is in contrast
to all finfish and invertebrate fisheries combined, where the
number of countries reporting catch has been largely stable over
the past 50 years (Fig. 1C). Although increasing trends in
invertebrate fisheries may be partly explained by increasing
precision in reporting (Fig. S2), there are clear underlying trends of
expansion by catch, country, and taxa (Figs. 1B, 1C, 2). This is
corroborated by studies on individual fisheries where assessments
or effort data are available [20,21].
The increase in invertebrate fisheries is driven not by a few
major target species, but instead by increasing catch trends across
all taxonomic groups (Fig. 2, Fig. S3). While catches have
increased continuously since the 1950s for more traditionally
fished crustaceans and bivalves, they rapidly increased in the
1980s and 1990s for often newly targeted cephalopods and
echinoderms. Thus, already existing fisheries expanded and new
fisheries were developed for species that had not been commer-
cially fished before. Although overall catch trends for invertebrate
fisheries paint a picture of continuing expansion (Fig. 1B), catches
in several groups (e.g., octopus and echinoderms) have slowed or
declined in recent years (Fig. 2B and 2D). The picture of universal
increase changes even more drastically if we look at individual
invertebrate fisheries by country. Here, some countries are still
expanding their catches while others peaked long ago (Fig. S4, see
also [5,21]).
Based on individual catch trajectories, we assessed the current
status and patterns of depletion of invertebrate fisheries. To do
this, we modified a technique of Froese and Kesner-Reyes [22] to
estimate the exploitation status of each invertebrate fishery from
catch data (Fig. S5). Our modifications overcome previous
weaknesses of this method by accounting for high variability in
catch, spurious peak catch years, and fisheries that are still
expanding (see Materials and Methods and Text S1). Our results
suggest that half of the fisheries had peaked as of 2004 (Fig. 3A),
with 18% fully exploited, 21% over-exploited or restrictively
managed, and 13% collapsed or closed with little difference across
functional groups (Fig. S6). This, combined with evidence of an
increasing number of countries reporting catch and an increasing
number of taxonomic groups targeted (Fig. 1C), indicates that the
globally increasing invertebrate catches (Fig. 1B) are likely supplied
by new taxa or new countries entering the fishery. In some
invertebrate fisheries, such as many sea cucumber fisheries [21],
decreasing catch trends have been directly related to population
declines; however, we do not suggest that catch trends are
generally good indicators of population status or have been driven
solely by high exploitation pressure. Declines in catch can also
have natural (e.g., recruitment failure due to climate) and other
human-related (e.g., changing markets, restrictive management)
drivers that can act in conjunction with each other [23].
Strong global markets may drive the expansion and serial
depletion of some fisheries over space and time [3,5,24],
particularly given the increasing availability of efficient fishing
gear, rapid global transport, and the incentive to preferentially fish
profitable marine resources [25]. If a fishery is declining in one
region, fishing companies move into other regions, usually further
away, to supply the demand of global buyers [5]. Some new
invertebrate fisheries have a single strong market, as shown for sea
urchins [5], where the global catch is related to the value of the
Japanese Yen [26]. For other taxa, single driving markets are less
obvious. For example, squid has 3 main importing nations (Japan,
Italy, and Spain), while others have even more (Text S1).
However, the vast majority of global sea cucumber catch is
exported to Hong Kong (64% by volume between 1950–2004) or
nearby Asian countries and the value of sea cucumbers has risen
dramatically in recent decades [27]. To test whether spatial
expansion has occurred, we used least-squares regression to
compare the great-circle distance from Hong Kong with the year
of peak sea cucumber catch for each country (Text S1) and found
a significantly positive relationship (r = 0.62, p = 0.002, Fig. 3B).
Given the generally poor stock status of sea cucumber fisheries
[27], this may indicate a strong driving market where fisheries are
sequentially exploited in relation to transportation distance. Such
serial exploitation can have strong negative social and ecosystem
consequences [5].
If markets and prices increase, new fisheries may develop more
rapidly over time. To test this, we compared the time when
invertebrate fisheries began or expanded with the time when they
reached an initial peak in catch (see Materials and Methods and Text
S1). We used an initial rather than overall peak in catch
trajectories to treat new and old fisheries equally. Despite
uncertainty within the results for individual taxa, we found a
significant overall reduction in time to peak for newer fisheries
(Fig. 3C). This corresponds to an approximate decrease of 6 years
(+3 years, 95% confidence interval) in time to peak when
comparing the 1950s to the 1990s. We suggest this may be a result
of better fishing technology combined with growing demand due
to the increasing global human population, changes in diet
preferences (e.g., the rise of sushi restaurants in Western countries),
declines in finfish fisheries, as well as more and more smaller
fisheries being exploited, facilitated by global transport. We note
that a pattern of serial depletion and substitution of other species
within each investigated taxonomic group could mask peaks in
catch [21] causing us to underestimate the rapid development of
fisheries. Where a peak in catch represents a peak in fishery
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productivity, it is unlikely that management and research can keep
up with this rate of expansion to ensure sustainable development
[5,6].
The rapid expansion, and in some cases serial depletion, of
global invertebrate fisheries may have strong ecosystem conse-
quences due to the method of fishing and the functional roles
invertebrates play in marine ecosystems. In 2000–2004, 53% of
invertebrate catch by volume and 71% by taxa fished were caught
by benthic trawling and dredging gear with these proportions
remaining relatively stable since the 1950s (Fig. 4A, B). This is
largely driven by benthic trawling for crustacean and cephalopod
species and dredging for bivalves. In comparison, benthic trawling
and dredging accounted for only 20% of global finfish catch (57%
of taxa, 2000–2004 mean). Such gear has substantive negative
impacts on most benthic habitats and communities by destroying
three-dimensional structure, impacting spawning and nursery
Figure 1. Spatial and temporal trends in catch, species diversity and countries involved in global invertebrate fisheries. (A) Mean
annual invertebrate catch in each Large Marine Ecosystem (LME) from 2000–2004. (B) Trends in invertebrate catch globally (red) and per country
(mean and standard error assuming a log-normal distribution, blue). Trends in all finfish and invertebrate catch (total catch, dashed red) are included
as a reference. (C) Trends in the number of countries reporting catch of invertebrates (solid red) and of all finfish and invertebrate species (total,
dashed red, as a reference) since the 1950s, and number of invertebrate taxa (taxonomic groups or species) fished by country (mean and standard
error assuming a negative binomial distribution, blue). Thickness of dark blue line approximates false increase due to increased reporting precision
(Text S1).
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grounds, altering benthic community composition, and reducing
future biomass, production, and species richness [28–30].
Moreover, together with mid-water trawls, benthic trawls and
dredges can incur a substantial portion of incidental by-catch [31].
Beyond the predator-prey roles that most finfish play in marine
ecosystems, invertebrates have more diverse functions and more
often provide essential ecosystem services such as maintaining
water quality [32,33], regenerating nutrients [34], providing
nursery and foraging habitat [35], and preventing algal over-
growth through grazing [36] (Fig. 4C). It has been shown that the
massive historic removal of oysters, such as in Chesapeake Bay,
was associated with increases in eutrophication and hypoxia [33].
We aggregated mean catch per year from 2000–2004 by
functional groups to assess the potential removal impact (Fig. 4D,
Table S4) (see Materials and Methods and Text S1). All invertebrate
taxa form potentially important roles as prey for higher trophic
levels while most cephalopods and crustaceans also perform
predatory roles. Especially bivalve, but also krill and some sea
cucumber fisheries, represent a substantial removal by volume (3
million t/year) of filter feeders. We estimate the removal of
bivalves alone to equate to a loss of *11 million Olympic-sized
swimming pools (*2:8:1010 m3) in filtering capacity per day in
2000–2004 (Text S1). In addition, many bivalves form beds,
banks, or reefs that structure the seafloor and provide important
habitat [35]. Invertebrate fisheries further remove *1:2million t
of detritivores and scavengers and *1:3million t of herbivores
annually. Although recruitment and re-growth will compensate for
some of these losses, the direct and indirect short- and long-term
ecosystem effects of these removals are largely unknown.
Our results demonstrate that despite overall increasing catches,
diversity, and country participation in global invertebrate fisheries,
there is strong evidence that the underlying trends in many
individual fisheries are less optimistic. Our new and more robust
analysis of catch trends suggests that an increasing percentage of
invertebrate fisheries may be over-exploited, collapsed, or closed.
Some invertebrate fisheries, such as the rock lobster fishery in
western Australia, have existed for a long time and are well-
managed [9], yet even there factors beyond the management
system, such as climate change, can present major challenges.
However, the same is not true for many newer fisheries like those for
sea urchins [5,12] and sea cucumbers [27] for which new fisheries
develop further away from their market(s) and at an increasingly
rapid rate, likely driven by strong market forces. This means that
global industries, markets, and free trade may enable the rapid
expansion of new fisheries before scientists and managers can step in
and make sensible decisions to secure the long-term, sustainable use
of these resources [5]. On the one hand, we risk losing some of the
last remaining viable and financially lucrative fisheries, bringing
financial and social hardship to a large number of small
communities dependent on these fisheries for income or food. At
the same time, the population and ecosystem consequences of many
invertebrate fisheries are largely unknown and unassessed [6],
although there are notable exceptions [8–11]. Whereas there is
increasing assessment, regulation, and rebuilding of finfish fisheries
to achieve more sustainable harvesting [7], many invertebrate
fisheries do not enjoy the same awareness or attention. Many of the
described patterns are reminiscent of an earlier phase in finfish
fisheries during which the rate of finding new fishing areas, new
Figure 2. Expansion of invertebrate catch since the 1950s across taxa. (A) crustaceans, (B) bivalves and gastropods, (C) cephalopods, and (D)
echinoderms. Upper lines indicate total catch for each group and underlying lines indicate catch for subgroups. Dark lines represent smooth
estimates obtained from a loess smoother (smoothing span 50% of the data). Light lines indicate the unfiltered catch trends.
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target species, and more efficient gears masked overall catch trends
[14]. However, because of improved industrial fishing gear and
global networks that allow rapid and accessible transport, we may
be progressing through invertebrate fishery phases even faster.
In order to prevent further uncontrolled expansion and instead
aim for a more sustainable development of invertebrate fisheries,
we highlight the need for a global perspective in their management
combined with local assessment, monitoring, and enforcement of
fisheries regulations. A global perspective is essential to identify
roving buyers, monitor foreign investments, and consider CITES
(U.N. Convention on International Trade in Endangered Species)
listing where appropriate [5]. Also, the displacement of fishing
effort from highly- to less-regulated regions and illegal, unreported,
and underreported (IUU) catches requires global regulations in
invertebrates and finfish fisheries alike [7]. On a regional and local
scale, stock assessments are infrequently or not performed for
many invertebrate fisheries and often lack adequate knowledge on
the species biology, population status, and response to exploitation
[6]. Invertebrates are rarely monitored in research trawl surveys
[7], and independent research surveys to assess population trends,
by-catch, and habitat impacts of invertebrate fisheries are rarely
done for many newer fisheries [5,6,12]. Based on such limited
knowledge, the sustainable exploitation of invertebrates for
fisheries may be difficult to achieve [13].
Figure 3. Status, drivers, and rate of development of invertebrate fisheries. (A) Estimated status of invertebrate fisheries over time as
expanding (green), fully exploited (yellow), over-exploited or restrictively managed (orange), and collapsed or closed (dark red/brown) based on catch
data. Light green indicates fisheries with less than 10 years of data at year of assessment. These fisheries were not evaluated. (B) Distance from Hong
Kong vs. year of first peak in catch for sea cucumber fisheries in different countries. Line represents least squares regression (r =0.62, p = 0.002), and
shaded area represents 95% confidence interval. Note that the analysis presented here differs from that reported in [21], see Text S1. (C) Meta-analysis
of correlation between fishery initiation year and time to peak catch across 10 invertebrate taxonomic groups. Dots represent median correlation
coefficients, lines represent 95% confidence intervals, and diamonds represent fixed (FE) and random effect (RE) pooled estimates (Text S1).
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Figure 4. Potential ecosystem effects of invertebrate fisheries. Habitat impacts expressed as (A) total invertebrate catch and (B, inset in A)
number of taxa fished by different gear types. (C) Ecosystem role of invertebrate taxa belonging to different functional groups and trophic levels (Text
S1). Dark and light blue indicate primary and secondary roles respectively (Text S1). (D) Removal impact expressed as total catch removed by
functional group as categorized in C (only the primary roles were included).
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In contrast, after many decades of increasing exploitation and fish
stock depletion, concerted management efforts in several regions
around the world achieved the reverse: a reduction in overall
exploitation rate and an increase in stock biomass in several finfish
fisheries [7]. This was achieved by a combination of management
tools adapted to local conditions as well as strong legislation and
enforcement. Similar measures can be implemented in invertebrate
fisheries to prevent current and future trajectories of depletion [10].
As an example, the addition of co-management and property rights
in Chilean artisanal gastropod fisheries solved many overexploita-
tion concerns, substantially increasing catch per unit effort and
mean individual size [11]. Similarly, the New Zealand rock lobster
fishery was on a path of declining abundance before a reduction in
effort and season length substantially increased abundance, catch
rates, and profitability [8]. Such successes provide a great
opportunity to inform the management of other newer fisheries. It
is our hope that increasing awareness of the ecological and
economic importance of invertebrates may spur more rigorous
scientific assessment, precautionary management, and sustainable
exploitation to ensure long-term resilience of invertebrate popula-
tions, ocean ecosystems, and human well-being.
Materials and Methods
Temporal and spatial catch trends
The Sea Around Us catch data are recorded by (i) country and
(ii) LME for which catches are assigned to 30630 minute cells
[37]. We mapped spatial patterns in global catches as the mean
annual invertebrate catch per 100 km2in each LME from 2000–
2004 (Text S1). We also mapped spatial patterns of global catches
for 4 major taxonomic groups (Fig. S1). Temporal trends from
1950–2004 were derived for overall invertebrate catch, total finfish
and invertebrate catch, and mean invertebrate catch per country
per year. Wherever possible, we corroborated the observed trends
with recent taxa-specific global reviews (Text S1).
Globally, over 1200 taxonomic groups and species are reported
caught in invertebrate or finfish fisheries, however, only the top
species are recorded individually by the Sea Around Us Project
with the remaining aggregated into groups such as ‘‘crustaceans’’
and ‘‘molluscs’’. We obtained catch data for a total of 302 ‘‘taxa’’
(including 213 species) and analyzed the number of taxa fished
over time, the number of countries fishing, and catch trends for 4
aggregated taxonomic groups (crustaceans, bivalves, echinoderms,
and cephalopods), and 12 species groups. To some extent, the
increasing diversity of taxa is a function of the increasing
taxonomic precision of reporting over time. Therefore, we
approximated the degree to which the increasing diversity
reflected a true trend of an increasing number of species being
targeted by fisheries (Fig. S2, Text S1).
The designation of countries can change over time; however,
such changes are reflected in the overall number of countries
reporting any catch for both finfish and invertebrate species, which
we included as a reference (Fig. 1C). Overall, the country
designation variation was small compared to the much larger
changes of increasing participation in invertebrate fisheries.
Nonetheless, we took this overall reporting trend into account
and scaled the number of countries reporting catch of different
invertebrate taxonomic and species groups to the total number of
countries fishing finfish or invertebrates in any given year (Fig. S3).
Assessment of fishery status from catch trends
Previous attempts have been made to categorize the status of
fisheries using catch data [1,22]. However, these approaches (i) can
incorrectly categorize a fishery as over-exploited or collapsed due to
single or multiple years of anomalous high catch and (ii) require all
non-declining fisheries to be categorized as fully-exploited by the
end of the time series. We developed a modified method for defining
fishery status designed to take into account these two shortcomings
by (i) applying a loess smoother to downweight outlying values and
(ii) allowing fisheries to remain expanding at the end of the time
series (Text S1). Further we assessed fishery status dynamically year-
by-year to treat old and new fisheries equally (Fig. S5, Text S1).
Dynamically evaluating the loess smoothed catches each year, a
fishery was considered ‘‘expanding’’ until there were at least 5 years
since a maximum in smoothed catch. A fishery was then defined as
‘‘fully-exploited’’. If smoothed catch increased again, a fishery
would be classified as ‘‘expanding’’. When smoothed catch was less
than 50% of a previous peak in catch,a fishery was defined as ‘‘over-
exploited’’. A fishery was defined as ‘‘collapsed or closed’’ when
smoothed catch fell below 10% of peak catch. We demonstrate the
robustness of our approach with simulated data (Fig. S7, Fig. S8,
Text S1).
Correlation of distance from Hong Kong
We were interested in testing whether some invertebrate
fisheries followed a pattern of spatial expansion and depletion
over time as has been shown for sea urchins [5]. Few species,
however, have a single strong market, making such detection
difficult. For sea cucumbers, the majority of catch is imported by
Hong Kong [21,38]. Thus we used the great circle distance
between Hong Kong and the largest cities in each country with a
sea cucumber fishery as a proxy for the transportation distance
between the importing and exporting nations. We separated the
US and Canadian east and west coasts because they are of
substantially differing distances from Hong Kong. We then related
log-transformed distance to the starting year of each fishery, which
we calculated as the year at which loess smoothed catch passed
10% of its first peak in catch (Fig. S9A, Text S1). See the
subsequent section Analysis of fishery development time for a description
of the calculation of the first peak in catch. We cross-checked the
starting years with published records (Table S2).
Analysis of fishery development time
We tested whether there was evidence that newer fisheries were
developing more rapidly over time by checking for a relationship
between when invertebrate fisheries began and the time when they
achieved their first peak in catch. Here, a fishery was defined as 1
of the 12 larger taxonomic groupings as reported by country
(Fig. 2). We excluded sea stars and krill due to the limited number
of countries with substantial fisheries. To focus on substantial
fisheries, we discarded all fisheries less than 1000 t/year, except
for lower-volume sea urchin and sea cucumber fisheries for which
we used a minimum catch of 250 t/year. Our overall conclusions
were invariant to choices of cutoffs from 500–2000 t (Text S1).
Catch trajectories can have multiple smaller local peaks together
with an overall peak. If we naively calculated the peak catch from
the entire available catch trajectory we would be more likely to be
measuring local peaks (rather than overall peaks) with fisheries that
started more recently. To avoid this time based bias we developed
a dynamic assessment method that calculated the time it took for
each fishery to develop to the first peak in catch (Fig. S9, Text S1).
For each year, we fit a loess curve to the data up to that year and a
fishery was considered to have reached a peak in catch if the
following conditions were true: (1) a maximum in catch occurred
and was less than 3 years from the end of the catch series at that
step, (2) a maximum in catch occurred that was at least 500 t for
most taxa or 125 t for echinoderms, and (3) the maximum in catch
was at least 10% greater than the catch at the current time step.
Global Invertebrate Fisheries
PLoS ONE | www.plosone.org 7 March 2011 | Volume 6 | Issue 3 | e14735
For fisheries that had yet to reach a peak in catch by the end of the
time series, we assigned simulated values based on the observed
times to a peak in catch for other fisheries (Fig. S10). We
repeatedly re-assigned these simulated values and evaluated the
correlation between year of initiation and time to the first peak in
catch. See Text S1 for further details.
Ecosystem effects
To assess the potential habitat effects of different invertebrate
fisheries, we calculated the total invertebrate catch and the
number of taxa fished by different gear types. The Sea Around Us
Project reports 19 types of fishing gear for invertebrates, which we
grouped into 6 broader groups based on their potential habitat
impact (Table S3, Text S1). To evaluate the potential food web
and ecosystem impacts of different invertebrate fisheries, we
assigned primary and secondary functional groups to larger species
groupings according to the primary literature and reference books
(Table S4). Trophic levels were obtained from the Sea Around Us
Project, where they were mainly derived from Froese and Pauly
[39]. We then assessed the overall removal of each primary
functional group as the total catch per functional group averaged
over 2000–2004. This does not include renewal of resources via
recruitment and re-growth. We also estimated the consequence of
removing filter-feeding bivalves from the ocean in more detail, in
terms of their capacity to filter water, using filtration rates reported
in the literature. We converted these values into Olympic-sized
swimming pools for comparison (Text S1).
Supporting Information
Text S1 Supplementary description of the methods.
Found at: doi:10.1371/journal.pone.0014735.s001 (0.15 MB
PDF)
Figure S1 Mean annual invertebrate catch by taxonomic group
in each Large Marine Ecosystem (LME) from 2000–2004.
Found at: doi:10.1371/journal.pone.0014735.s002 (1.13 MB TIF)
Figure S2 Effects of taxonomic precision in reporting on
predicted trends in diversity of invertebrates fished. (A) Increasing
reporting of invertebrate taxa fished divided into species level
(blue), larger grouping level (green), and combined (red). Dark
lines represent mean and shaded region represents standard error
assuming a negative binomial distribution of the data. (B–D)
Estimated mean number of invertebrate taxa fished per country
assuming different penalties for increased taxonomic precision.
Dark blue line indicates estimate, light blue shaded region
indicates standard error assuming a negative binomial distribution
of the data, and the dark blue shaded regions indicate an estimated
trend adjusted for increasing taxonomic precision in reporting. (B)
Assumes each loss of an aggregated group results in 2 new species
level designations, (C) assumes 3, and (D) assumes 4.
Found at: doi:10.1371/journal.pone.0014735.s003 (0.24 MB TIF)
Figure S3 Percentage of all countries reporting catch of various
invertebrate taxonomic and species groups. Dark lines represent
smooth estimates obtained from a loess smoother (smoothing span
50% of the data). Light lines represent unfiltered data.
Found at: doi:10.1371/journal.pone.0014735.s004 (0.28 MB TIF)
Figure S4 An example invertebrate catch series arranged by
country for one invertebrate taxa: bivalves. Red lines indicate loess
smoothed fits. Plots are ordered by cumulative catch since 1950.
Vertical grey bars in title bars indicate log transformed cumulative
catch, with bars near the right indicating the greatest cumulative
catch and bars near the left indicating the least cumulative catch.
Found at: doi:10.1371/journal.pone.0014735.s005 (0.69 MB TIF)
Figure S5 Illustration of our algorithm for dynamically assigning
fishery status. Dots represent raw catch values, grey lines represent
3 of the loess functions fit to the data. Loess functions were built
dynamically for each year but for clarity we show only the 3
functions which resulted in a change in status. By default a fishery
was categorized as ‘‘expanding’’ until one of the following criteria
was met: when there was at least 5 years since a maximum in the
smoothed catch the fishery was classified as ‘‘fully exploited’’,
when smoothed catch fell below 50% of maximum smoothed
catch the fishery was classified as ‘‘over-exploited’’, and when
smoothed catch fell below 90% of maximum catch the fishery was
classified as ‘‘collapsed or closed’’.
Found at: doi:10.1371/journal.pone.0014735.s006 (0.17 MB
TIF)
Figure S6 Percentage of fisheries for species from various
functional groups that were categorized into the 4 fishery status
categories. See section Assessment of fishery status from catch trends and
Fig. 4C for a description of the how the species were assigned to
the functional groups.
Found at: doi:10.1371/journal.pone.0014735.s007 (0.18 MB
TIF)
Figure S7 Demonstration of our fishery status assessment
algorithm to simulated data. (A–C) Example of simulated
increasing and then stationary catch series with multiplicative
log-normal error about a random mean: log standard deviation of
error of 0.10 (A), 0.25 (B), and 0.50 (C). Black lines indicate
unfiltered catch. Red lines indicate loess smoothed fits. (D–F)
Predicted stock status (expanding = green, fully exploited = yellow,
over-exploited or restrictively managed = orange) from simulated
data showing the robustness of our method to variability in the
data as indicated for A, B, and C, respectively.
Found at: doi:10.1371/journal.pone.0014735.s008 (0.25 MB TIF)
Figure S8 Characteristics of actual and simulated catch series.
Frequency of log of mean catch values by fishery and log of the
standard deviation of the residuals after fitting a loess smoother to
each series (span = 0.5) from global invertebrate fisheries (A, B;
grey background shading), and simulated series with s= 0.1 (C,
D), s= 0.25 (E, F), and s= 0.5 (G, H). See section Verification of
fishery status estimation using simulated data for a description of s. Red
and blue vertical lines indicate median values.
Found at: doi:10.1371/journal.pone.0014735.s009 (0.39 MB
TIF)
Figure S9 Methods used to determine years of initial peaks in
catch. (A) Illustration of our algorithm for assigning year of initial
peak catch. Dots represent raw catch values, grey line represents
loess function fit through the entire catch series, and red line
indicates loess function fit through data up to the year of initial
peak catch. A fishery was considered to have peaked if there was at
least 500 tonnes of catch, at least a 10% decline from peak catch,
and at least 3 years of data after the peak in catch. This algorithm
was applied dynamically each year until the first instance of peak
catch was observed. (B) Illustration of sampling time to peak for
one censored fishery (Fishery A, red circle). Fisheries for which
time to peak could be calculated are shown with solid dots in the
shaded blue triangle. Censored fisheries for which time to peak
was sampled are shown with open dots. Vertical dashed line
indicates known year in which Fishery A surpassed 10% of its
maximum observed catch. Fishery A could therefore have been
assigned a time to peak from any value above 10 years, as
indicated by a horizontal dashed line, and before 1970 (dark blue
shaded region). This sampling was repeated 1000 times.
Global Invertebrate Fisheries
PLoS ONE | www.plosone.org 8 March 2011 | Volume 6 | Issue 3 | e14735
Found at: doi:10.1371/journal.pone.0014735.s010 (0.25 MB TIF)
Figure S10 An example of time to peak catch vs. year of fishery
initiation by taxonomic grouping for one random sampling of
censored fisheries (red dots). Black dots represent known data
points. In our analysis, the red dots were resampled 1000 times
from possible time to peak values. Blue dots represent fisheries for
which there were no fisheries to sample from. These were set to
the maximum observed number of years for the earliest fishery
affected (the left-most blue dot).
Found at: doi:10.1371/journal.pone.0014735.s011 (0.34 MB TIF)
Table S1 Invertebrate catch for the 6 LMEs with the greatest
total catch from 2000–2004. Also shown are the 3 taxonomic
groups within each LME with the greatest catch. Catch values
shown are annual averages over the 5-year span. LMEs are
ordered by decreasing catch and within the LMEs the taxonomic
groups are ordered by decreasing catch of that taxon.
Found at: doi:10.1371/journal.pone.0014735.s012 (0.03 MB
PDF)
Table S2 Distance and starting year of sea cucumber fisheries by
country. Listed are each country’s largest city (by population), its
location, its distance from Hong Kong, the starting year of the sea
cucumber fishery, and a verification reference.
Found at: doi:10.1371/journal.pone.0014735.s013 (0.09 MB
PDF)
Table S3 Major gear groupings of gear categories from the Sea
Around Us Project catch database.
Found at: doi:10.1371/journal.pone.0014735.s014 (0.03 MB
PDF)
Table S4 Classification of invertebrate taxonomic groups into
primary and secondary functional groups. Taxa are ordered
approximately by decreasing trophic level.
Found at: doi:10.1371/journal.pone.0014735.s015 (0.05 MB
PDF)
Acknowledgments
We thank T.A. Branch, R.I. Perry, N.L. Shackell, B. Worm, E.L. Hazen,
and 2 anonymous reviewers for comments that greatly improved this
manuscript. W. Blanchard and C. Field provided helpful statistical advice
and discussions on the methods.
Author Contributions
Conceived and designed the experiments: SCA JMF HKL. Analyzed the
data: SCA JMF HKL. Contributed reagents/materials/analysis tools: RW.
Wrote the paper: SCA JMF RW HKL.
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Global Invertebrate Fisheries
PLoS ONE | www.plosone.org 9 March 2011 | Volume 6 | Issue 3 | e14735

Supplementary resources (15)

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