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Assessing the changing biodiversity of exploited marine ecosystems
1 2,3
Lynne Shannon and Marta Coll
Marine biodiversity and ecosystem functioning have changed Several ecological indicators have been identified to assist
and are continuing to change in marine ecosystems across the us in measuring the capacity of marine ecosystems to
world. These changes are driven by human interactions with deliver ecosystem services [4]. Species interactions, as
the environment and ecosystems, as well as by natural opposed to merely the numbers and abundance of spe-
environmental change, both locally (at the ecosystem level) and cies, have been identified as the key ‘fabric’ in determin-
globally. This paper draws on published research, in particular ing how an ecosystem responds to a pressure like fishing
that using ecosystem indicators to identify, assess and [5]. It is for this reason that food-web-related measures
compare changes in biodiversity of exploited marine have been highlighted as crucial in our understanding and
ecosystems across the globe. We use our results to reflect on predicting of how marine biodiversity is and may change
the sustainability of our changing exploited marine ecosystems in the future [6,7]. Fisheries management measures may
and consider ways forward to incorporate this information in well benefit biodiversity of an ecosystem in terms of
decision making processes. maintaining size structure of the fish community, for
example, but food-web structure and function may not
be well maintained through adopted management mea-
Addresses
1 sures that alter abundance of the different feeding guilds
Marine Research Institute and Department of Biological Sciences,
in a food web [8 ].
University of Cape Town, Private Bag X3, Rondebosch, Cape Town
7701, South Africa
2
Institute of Marine Science (ICM-CSIC), passeig Marı´tim de la
Fishing is acknowledged as a major driver of changes in
Barceloneta, n 37-49, 08003 Barcelona, Spain
3 marine ecosystems [9] and is our focus in this article.
Ecopath International Initiative Research Association, Barcelona, Spain
Removal of top predators, keystone species, or important
Corresponding author: Shannon, Lynne ([email protected]) prey species changes biodiversity and in particular eco-
system functioning [10]. We are fishing marine food webs
in several ways. Top predators and larger species and
Current Opinion in Environmental Sustainability 2018, 29:89–97
individuals [11] are removed from ecosystems; we are
This review comes from a themed issue on Environmental change
fishing down the food web [12]. We are also fishing
issues
through the food web by removing larger species and
Edited by Debra Zuppinger-Dingley, Cornelia Krug, Owen Petchey,
fish while simultaneously adding smaller species and fish
Bernhard Schmid, Norman Backhaus and Michael E Schaepman
to the basket of exploited species [13], and fishing up the
food web by adding to catches those of high trophic-level
Received: 18 August 2017; Revised: 17 January 2018; Accepted: 20 species [14]. In addition, we are fishing at greater depths
January 2018
over time [15]. Monitoring the mean trophic level of
species that are caught is a useful indicator in a suite
https://doi.org/10.1016/j.cosust.2018.01.008 of indicators that are being employed to detect ecosystem
changes and losses in marine biodiversity due to fishing
1877-3435/ã 2018 Published by Elsevier B.V.
[16,17 ,18]. Marine food web models combine multiple
species or functional groups and are the basis to represent
the more complex relationships and interactions within
marine ecosystems. Thus, ecological indicators from food
web models have been highlighted as useful tools to
quantify ecosystem effects of fishing ([19]) and can be
How is marine biodiversity changing?
used to analyse emerging food-web properties and
Biodiversity is usually considered to be a representation
changes in food-web structure and functioning in time
of species diversity within an ecosystem. However, other
and space [20].
aspects of biodiversity are well recognized, including
genetic diversity, ecosystem diversity and functional
diversity (e.g. [1–3]). In particular, the ability of marine Climate-induced geographic shifts in distributional
ecosystems to function in ways that are conducive to ranges of marine species are also a significant driver of
provisioning (e.g. catches) and regulating (e.g. climate biodiversity change across the world. For example, Pinsky
et al.
influences) ecosystem services is highly desirable in our [21] examined the rate and direction of climate
changing world with an ever expanding human popula- change off the North USA coast between 1968 and 2011,
tion needing sustenance and quality of life. showing that climate velocity explains the spatial shift in
www.sciencedirect.com Current Opinion in Environmental Sustainability 2017, 29:89–97
90 Environmental change issues
marine species. Brander [22] reviewed climate change Using a carefully-selected suite of seven ecological indi-
impacts on marine ecosystems and fisheries, predicting cators to measure the ecosystem effects of fishing [31,32],
that under a scenario of a 2 C temperature rise above pre- various methods were used to assess the status of
industrial levels, spatial shifts in marine species with exploited marine ecosystems [33 ]. Ecosystems were
implications for species richness, would increase in ranked according to how the indicators compared in terms
mid-high latitudes and decrease in the tropics by of recent ecosystem state and trends over time [27 ,34],
2050. As a result of species’ thermal preferences, inva- and ecosystem status compared by means of decision
sions would be likely to occur at high latitudes and local trees that sequentially considered indicator trends [35].
extinctions are predicted for the tropics and semi- More recently, an additional five ecological indicators
enclosed seas [22]. Detailed regional studies are being (Table 1) were identified to capture the broader biodi-
done in this regard. For example, Hare et al. [23] present a versity aspects of ecosystem changes due to fishing [27 ].
trait-based assessment of the vulnerability of marine Using this second, complementary set of biodiversity-
species along the Northeast US coast to climate change. focussed indicators, 27 exploited marine ecosystems cov-
Ben Rais Lasram et al. [24] predict that several endemic ering an array of ecosystem types from around the world
fish species will be at risk or go extinct in the Mediterra- were compared according to ecosystem state averaged
nean Sea due to future sea surface temperature rise and an over the years 2005–2010, and ecosystem trends from
extensive fragmentation of their range sizes. In addition 1980 to 2010, or for as long as the data were available in an
to physiological impacts, indirect effects of climate ecosystem (Table 2; Figures 1 and 2). This assessment
change manifest throughout the marine food web, not highlighted the worrying deteriorating trends in biodiver-
least being shifts in abundance and distribution of sea- sity in several marine ecosystems, and the poor status of
birds and marine mammals, which are better able to cope biodiversity compared to averages across assessed ecosys-
with thermal changes than most fish species, yet depen- tem case studies. The study also exposed the different
dent on prey distributions [25]. All in all, spatial changes parts played by multiple pressures (e.g. fishing, the envi-
in species’ distributions will have implications for fisher- ronment [36], and human dimensions [37] such as market
ies and ecosystems. In fact, a 3–13% decrease in global forces) acting together to determine observed dynamics
catch potential is predicted by 2050 under a high green- (measured by the ecological indicators) in marine ecosys-
house gas emissions scenario [26 ]. tems and the frequent non-linear responses of these
indicators. Overall, it showed the value in ensuring that
Status of marine biodiversity inferred from broader, biodiversity-focussed indicators are considered
ecological indicators in addition to single-species/population metrics and more
We draw on two groups of recent studies that report on impact-focussed ecosystem indicators. The need for
global (marine) biodiversity changes. Both rely on suites informed, expert-driven interpretation of observed indi-
of indicators to monitor strength of a pressure (such as cator trends was particularly noteworthy [17 ,27 ].
fishing) in an ecosystem, and responses of the ecosystem
to such pressures. These were selected as they were Global assessments
recently published and span two opposite scales of assess- The Ocean Health Index [28 ] was developed to assess
ment — the comparative approach across exploited the health of human–ocean coupled systems through the
marine ecosystem case studies (focussing on [27 ]) and lens of benefits to people. Although not specifically
global assessment (e.g. [28 ]) of progress made towards focussed on biodiversity assessment as such, the index
improving biodiversity status including the marine realm does measure the current status and likely future state of
[29 ]. ten goals: food provision, artisanal fishing opportunity,
natural products, carbon storage, coastal protection, tour-
Comparative ecosystem study ism and recreation, coastal livelihoods and economies,
Marine ecosystems are inherently complex and ecological sense of place, clean waters and biodiversity. The index
indicators can help describe them and their changes in was first globally applied and indicated a medium perfor-
simpler terms. Commonly used indicators include species mance of countries globally, with only 5% of countries
occurrence and abundance, functional group presence scoring higher than 70 (in a range from 0 to 100) and 32%
(such as feeding types, habitat builders or filter feeders), scoring lower than 50. Food provision, closely related with
as well as species traits such as body size or trophic fishing impacts, was one of the goals that ranked lowest
ecology [30]. These are used to analyse changes in overall. Since the global application, the index has been
individual populations or across multiple species over applied in different countries to raise public awareness,
time, thereby providing insight into changes in marine direct resource management, improve policy and priori-
species and ecosystems. Global comparisons have been tize scientific research (e.g. [38], http://www.
made across marine ecosystems using ecological indica- oceanhealthindex.org).
tors, represented as trend lines or slopes of trends (over
time), heat maps and petals plots (e.g. [27 ]; In 2002, the CBD (Parties to the Convention on Biologi-
Figures 1 and 2). cal Diversity) committed to making substantial progress
Current Opinion in Environmental Sustainability 2017, 29:89–97 www.sciencedirect.com
Assessing changes in marine biodiversity Shannon and Coll 91
Figure 1
Indiseas 2 BarentsS 0.071 0.071 -0.023 0.02
BiscayB 0.021 -0.039 0.041 0.026
BlackS -0.041 0.028 -0.027 -0.06
CBalticS -0.081 -0.021 -0.067 -0.045
ChathamR 0.069 -0.016 -0.109
EBeringS -0.08 0.017 0.012
EEnglishC -0.054 -0.057 0.036 EScotianS 0.046 -0.07 -0.07
GuineaS -0.008 0.113 -0.035 -0.107
GoC -0.081 -0.043 0.035 -0.398
GoG -0.018 -0.131 0.513
GoL 0.27 0.1 -0.043
IrishS 0.079 -0.09 -0.064 Slope Coefficients NAegeanS -0.09 0.039 -0.49 0.741 Neg Sig NlonianS 0.015 -0.034 0.091 0.089 Neg Non-Sig Pos Non-Sig NorthS 0.052 -0.057 -0.035 -0.054 0.032
Pos Sig
Ecosystem NCAdriaticS 0.01 -0.077 -0.077 0.028 -0.062
NEUS -0.043 -0.085 0 NHumboldtC -0.117 -0.119 -0.089 -0.199
PortugalC -0.016 -0.077 -0.042
PEI -0.145 -0.173
SaharaC -0.055 SenegalS -0.08 0.072 0.058
SBenguela -0.266 0.022 -0.067 -0.122
SCatalanS 0.071 0.075 -0.015 -0.088
WCScotland -0.12 -0.106 -0.081 0.125 -0.039
WCUS -0.073 0.065 -0.389
WCVancouverl -0.041 -0.013 0.002 0.177
WScotianS 0.078 -0.074 0.039 -0.049 D IVI MTI TLsc TLmc
Current Opinion in Environmental Sustainability
Heatmap of the slope coefficients of biodiversity indicator trends (‘IndiSeas Phase II’) fitted for 1980–2010 using a generalized least-squares and
autoregressive error analysis (assuming linearity over time). Neg: negative, Pos: positive, Sig: significant, Non-Sig: non-significant trend. Indicator
abbreviations on the plots are as follows: mean intrinsic vulnerability (IVI); non-declining species (NDES); Marine Trophic index (MTI); trophic level
of the community (TLsc); trophic level of the model (TLmc); landings/discards (D). Ecosystems from top to bottom: Barents sea, Bay of Biscay,
Bering Sea, Black Sea, Central Baltic Sea, Chatham Rise, East English Channel, Eastern Scotian shelf, Guinean EEZ, Gulf of Cadiz, Gulf of Gabes,
Gulf of Lions, Inner Ionian Sea, Irish Sea, Morocco (Sahara coastal), North Aegean Sea, North Sea, North-central Adriatic Sea, North Eastern USA,
Northern Humboldt (Peru), Portuguese EEZ, Prince Edward Island, Senegalese EEZ, Southern Benguela, Southern Catalan Sea, USA West Coast,
www.sciencedirect.com Current Opinion in Environmental Sustainability 2017, 29:89–97
92 Environmental change issues
Figure 2
Barents Bering Biscay BlackS Catalan CBaltic
Chatham EChannel EScotianS GoC GoG GoL Guinea lonian Irish Morocco NAegean NCAdriatic Indicator D MTI NDES TLmc TLsc
NEUS NHumboldt NorthSea PEI Portugal SBenguela
Senegal USAWCoast WCScotland WCVancouverl WScotianS
Current Opinion in Environmental Sustainability
Petal plots comparing values of biodiversity state indicators averaged for the period 2005–2010. Indicator values are scaled as a proportion of the
range of indicator values across ecosystems examined. Indicator abbreviations on the plots are as follows: mean intrinsic vulnerability (IVI); non-
declining species (NDES); Marine Trophic index (MTI); trophic level of the community (TLsc); trophic level of the model (TLmc); landings/discards
(D). Ecosystems from top to bottom: Barents sea, Bay of Biscay, Bering Sea, Black Sea, Central Baltic Sea, Chatham Rise, East English Channel,
Eastern Scotian shelf, Guinean EEZ, Gulf of Cadiz, Gulf of Gabes, Gulf of Lions, Inner Ionian Sea, Irish Sea, Morocco (Sahara coastal), North
Aegean Sea, North Sea, North-central Adriatic Sea, North Eastern USA, Northern Humboldt (Peru), Portuguese EEZ, Prince Edward Island,
Senegalese EEZ, Southern Benguela, Southern Catalan Sea, USA West Coast, West Coast Vancouver Island, West Coast Scotland, Western
Scotian Shelf.
Source: Figure from [27 ].
by 2010 in curbing the rate of biodiversity loss across the more dramatic action [41]. Progress towards meeting the
world’s diverse ecosystems [39]. Unfortunately, this goal 20 ‘Aichi Targets’ for biodiversity has been assessed mid-
was not well achieved globally [40], and the Strategic Plan way through this decade [29 ]. Tittensor et al. [29 ]
for Biodiversity was adopted for 2011–2020, calling for examined time series of a carefully-selected suite of
(Figure 1 Legend Continued) West Coast Vancouver Island, West Coast Scotland, Western Scotian Shelf.
Source: Figure modified from [27 ].
Current Opinion in Environmental Sustainability 2017, 29:89–97 www.sciencedirect.com
Assessing changes in marine biodiversity Shannon and Coll 93
Table 1
The set of complementary biodiversity-based ecological indicators identified in the IndiSeas project.
Biodiversity indicator Label (abbreviation) Used for state (S) or trend (T)
Mean intrinsic vulnerability index of the fish landed catch Mean vulnerability (IVI) T
Proportion of non-declining exploited species Non-declining species (NDES) S
Catch-based marine trophic index Trophic index (MTI) S, T
Mean trophic level of the surveyed community Trophic level of the community (TLsc) S, T
Mean trophic level of the modelled community Trophic level of the model (TLmc) S, T
Proportion of discards in the fishery Landings/discards (D) S, T
Source: Taken from [27 ].
Table 2
Status of marine ecosystems determined using biodiversity-focussed indicators listed in Table 1. State is assessed by comparing scaled
indicator values relative to average across the ecosystems and provided in the first three columns. Trends are assessed according to
generalized linear modelling accounting for autocorrelation, shown in columns 4–6. The remaining 14 ecosystem case studies not listed
in columns 4–6 showed no clear trends in biodiversity indicators between 1980 and 2010. Assessments are those reported in [27 ].
Below ecosystem Above ecosystem Contrasting patterns Declining trends Increasing trends Mixed trends
average (state) average (state) across indicators (state)
Black Sea Barents Sea Central Baltic Central Baltic Barents Sea Irish Sea
Gulf of Cadiz Bay of Biscay Guinean Shelf E. Scotian Shelf N. Ionian Sea N. Aegean Sea
N. Aegean Sea Catham Rise Gulf of Gabes N-Central Adriatic N. Humboldt Current
N. Ionian Sea E. Bering Sea Irish Sea Portuguese Coast Senegalese Coast
N-Central Adriatic Sea E. English Channel W. Coast of Scotland Prince Edward S. Catalan Sea
Islands
N. Humboldt Current E. Scotian Shelf W. Scotia Shelf W. Coast of Scotland
Senegalese Coast Gulf of Lyons W. Scotian Shelf
S. Catalan Sea North Sea
NE US
Portuguese Coast
S. Benguela
W. Coast US
W. Coast Vancouver
Island
indicators of progress towards 16 of the 20 Aichi Targets. established in 2012 and is facilitating enormous efforts in
Indicators were identified to measure progress in addressing policy and management needs underpinning
responding to losses in biodiversity, improving state of maintenance of biodiversity in ecosystems worldwide; it
ecosystems, reducing pressure on ecosystems and is the biodiversity equivalent of the well-known Inter-
enhancing benefits for humans of improved biodiversity, governmental Panel on Climate Change (IPCC). Nature,
and model projections were made to 2020. The authors its benefits to/impacts on humans, its drivers and gover-
reported that overall responses by society to loss of nance systems have been carefully incorporated into an
biodiversity have been improving in the past few decades, overarching ‘conceptual framework’ for IPBES [42].
whereas the state of ecosystems with respect to biodiver- From here, international, collaborative work is underway
sity was declining overall, and the pressures acting on to prepare regional and global assessments of biodiversity
ecosystems and contributing to declines in biodiversity in terms of state, pressures, benefits (or contributions)
have been increasing in strength. Homing in on the amongst other aspects behind the value of biodiversity to
marine-specific indicator series considered, marine bio- humans.
diversity state is notably deteriorating (Table 3, ‘State’
and ‘Pressure’ indicators), but societal effort has been According to recent research on marine biodiversity
harnessed in an attempt to address this issue (Table 3, changes, it is recommended that assessment of
‘Response’ indicators). Considering these results, it is marine ecosystem status be undertaken by means
unlikely that the goals for 2020 will be achieved. of a suite of indicators, as opposed to one or two all-
encompassing indicators [17 ,27 ,32,34]. This re-
Taking these findings forward into decision- commendation rests on the careful identification of
making processes indicators that correctly measure different ecosystem
The Intergovernmental Platform on Biodiversity and properties, pressures, ecosystem responses and manage-
Ecosystem Services (IPBES; http://www.ipbes.net) was ment objectives. Therefore, using a suite of indicators
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94 Environmental change issues
Table 3
Trends in global marine biodiversity indicators reported by [29 ]. Time periods extend from the 1950s (or earliest year for which data are
available), to 2010 or 2013 (latest year for which data were available at time of the assessment), and model projections were done to
2020. Worsening of the situation with respect to biodiversity is indicated by means of shaded cells.
Biodiversity indica tor Measure of ecosystem Trend
state, response to
biodiversity loss, or
press ure acting to reduce
biodiversity
Coral ree f cover State Declining
Red List Index for Sea birds State Declining
Fish stocks within safe State Declining
biologica l limits
Global eff ort in bottom Pressure Increasing
trawli ng
Funding for institutional Responses Increasing
capac ity building in
fisheries
Tonn age of Marine Response Increasing Stewardship Council-
engaged fisheries
Protec ted area coverage of Response Increasing
marine ecoregions
Global coverage of marine Response Increasing
protec ted areas
provides a fuller picture of ecosystem impacts, responses indicators. An example is the work by Lockerbie et al.
and status. [47 ,48,49], whereby ecological indicators are differen-
tially weighted according to significance of trends over
However, assessing marine ecosystems based on multiple time and the extent of the influence of fishing versus
ecological indicators is complicated and decision makers environmental conditions in the particular ecosystem and
are often left to grapple with varied and contrasting period (Figure 3). This work heavily integrates local
ecosystem trends and values, with little guidance as to knowledge of the ecosystem processes, the physical envi-
what these signals mean and the implications thereof. ronment and historical fisheries management strategies,
There is thus a dire need for more scientific effort to be to arrive at a better informed assessment of ecosystem
put into developing decision support tools. In other status to inform decision makers. This entailed careful
words, the information that is integrated into indicators consultation with local ecosystem experts, and subse-
needs further synthesis and interpretation. For example, quent adjustment of individual time periods to capture
this has been attempted by means of scoring-based environmental regimes, and of indicator trends to capture
assessments to rank marine ecosystems according to correct interpretations that incorporate, for example dis-
fishing impact [43]. Another example is the development card and unreported catch in the case of the Catalan Sea
of decision trees that invoke one or several indicators at a [48], or ecosystem responses to serious management
time, sequentially leading one through a process that measures implemented in the North Sea [49].
arrives at an overall assessment of ecosystem status
[35,44,45]. Novel approaches are needed to synthesize ecological
information (such as that provided by indicators) in ways
Decision trees such as these offer themselves to being that incorporate the fullest extent of our understanding of
extended into formal ‘expert systems’ — user-interfaced ecosystem processes and responses to pressures, and need
decision tree frameworks that guide stakeholders through to account for epistemic (spatial and temporal variability
a series of rule-based decisions, providing background [18], data gaps, among others) and linguistic (related to
and reasoning for decisions based on indicator trends, to scientific definition) uncertainties [50], with regular
arrive at an ecosystem assessment (e.g. see [45,46]). updates being undertaken. As is also called for in ([51,
Recently, more nuanced frameworks are being explored this issue]), this will allow us to equip decision makers to
whereby local ecosystem characteristics and histories are make more informed decisions towards managing pres-
more formally accounted for in interpreting multiple sures that alter marine biodiversity, in that way
Current Opinion in Environmental Sustainability 2017, 29:89–97 www.sciencedirect.com
Assessing changes in marine biodiversity Shannon and Coll 95
Figure 3
3. Envi ronmental indicators
1. Ecologi cal Indicators
To wha t extent does the condition of the
Trends in each ecological indicator env ironment explain trends observed in each
(based on those reported in Shin et ecological ind icator?
al. 2010 and Collet al.2016) are
scored according to significance and Redu ce/slightly reduce revised indicator score if
direction of change (linear trends envi ronmental conditions explain/partially explain)
fitted) over a given time period the obse rved trend; no further change in indictor
score if no influence of environment on the
2. Fishing pressure indicators indicator in the period examined
Output: final indicator scores
To wha t extent does the trend in fishing
pres sure explain the observed trend in
each ecological ind icator?
Increase/sli ghtly increase the weighting 4. Ecosystem status assessment
of indicator if fishing explains/partially
explains the trend ; no change in indicator Revised scores are averaged (weightings adjusted for
score if no influence of fishing on the redundancy in indicators) to categorise ecosystems
ind icator in the period examined. as: improving, possibly improving, deteriorating,
Outpu t: revised indicator scores possibly deteriorating, or showing no improvement or deterioration over the time period exam ined
Current Opinion in Environmental Sustainability
Conceptual diagram of the decision tree framework developed by [47 ] to categorize ecosystem status according to ecological indicator scores
and fishing and environmental pressures.
encouraging the healthy functioning of marine ecosys- Acknowledgements
tems beyond individual species. In this article we have
LJS is grateful for funding and the support of the South African Research
focussed on fishing as a key driver of biodiversity changes Chair Initiative (SARChI), funded through the South African Department
and have highlighted some of the recent thinking and of Science and Technology (DST) and administered by the South African
National Research Foundation (NRF) and hosted by the University of Cape
studies behind improving the way we feed our scientific
Town. MC was partially funded by the European Union’s Horizon research
understanding and monitoring into management pro- program grant agreement No. 689518 for the MERCES project. Participants
of the EUR-OCEANS IndiSeas project (www.indiseas.org) are
cesses for the benefit of maintaining healthy, diverse
acknowledged for their contributions towards a comparative global fisheries
marine ecosystems. Similar efforts should address other
indicator study drawn heavily upon here.
drivers of change of marine ecosystems, so that unified,
combined ecosystem assessments of biodiversity can be
made, and appropriate societal responses encouraged. In References and recommended reading
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of special interest
based’ social–ecological research dealt with in ([52, this
of outstanding interest
issue]), have emphasized deterioration of ecosystems
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