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Assessing the changing of exploited marine

1 2,3

Lynne Shannon and Marta Coll

Marine biodiversity and 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 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 of our changing exploited marine ecosystems in the future [6,7]. 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 , 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 [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, , 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 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]. 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 within an ecosystem. However, other

and space [20].

aspects of biodiversity are well recognized, including

genetic 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 , 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

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



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, 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

[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 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

www.sciencedirect.com Current Opinion in Environmental Sustainability 2017, 29:89–97

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

Papers of particular interest, published within the period of review,

summary, the local ecosystem-scale assessments dis-

have been highlighted as:

cussed here, and which fall into the category of ‘place-

 of special interest

based’ social–ecological research dealt with in ([52, this

 of outstanding interest

issue]), have emphasized deterioration of ecosystems

with respect to ecosystem status and biodiversity

 1. Gaston KJ: Global patterns in biodiversity. Nature 2000,

[27 ]. Global scale assessments have similarly shown 405:220-227.

declines in biodiversity resulting from increasing pres- 2. Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E: The



influence of functional diversity and composition on

sures being exerted on marine ecosystems [29 ]. How-

ecosystem processes. Science 1997, 277:1300-1302.

ever, it is encouraging that society is at least putting



3. McCann K: Protecting biostructure. Nature 2007, 446 29-29.

increased effort into addressing these threats [29 ], leav-

ing us with some hope that our marine ecosystems can 4. Kleisner K, Coll M, Lynam CP, Bundy A, Shannon L, Shin YJ,

Boldt J, Borgesi MF, Diallo I, Fox C et al.: Evaluating changes in

eventually be sustainably managed.

marine communities that provide ecosystem services through

comparative assessments of community indicators. Ecosys

Serv 2015, 16:413-429.

Conflicts of interest 5. Travis J, Coleman FC, Auster PJ, Cury PM, Estes JA, Orensanz J,

Peterson CH, Power ME, Steneck RS, Wootton JT: Integrating

There are no known conflicts of interest to declare with

the invisible fabric of nature into fisheries management. Proc

respect to this article. Natl Acad Sci 2014, 111:581-584.

www.sciencedirect.com Current Opinion in Environmental Sustainability 2017, 29:89–97

96 Environmental change issues

6. Janzen DH: The deflowering of Central America. Nat Hist 1974, 25. Sydeman WJ, Poloczanska E, Reed TE, Thompson SA: Climate

83:48-53. change and marine vertebrates. Science 2015, 350:772-777.

7. Cury PM, Shannon LJ, Roux JP, Daskalov GM, Jarre A, 26. Cheung WW, Jones MC, Reygondeau G, Stock CA, Lam VW,



Moloney CL, Pauly D: Trophodynamic indicators for an Fro¨ licher TL: Structural uncertainty in projecting global

ecosystem approach to fisheries. ICES J Marine Sci 2005, fisheries catches under climate change. Ecol Model 2016,

62:430-442. 325:57-66.

Models of future climate change scenarios are used to project catch

8. Lynam CP, Mackinson S: How will fisheries management potential across the globe under different levels of uncertainty, and



measures contribute towards the attainment of good project a decline of between 3 and 13% in global catch potential by

environmental status for the North Sea ecosystem? Global 2050 under the ‘high emission scenario’.

Ecol Conserv 2017, 4:160-175.

Fishing strategies addressing MSY targets are modelled and suggest that 27. Coll M, Shannon LJ, Kleisner KM, Juan Jorda` MJ, Bundy A,



although beneficial to fish communities in terms of size of fish, food web Akoglu G, Banaru D, Boldt JL, Borges MF, Cook A et al.:

traits such as community evenness and trophic structure may suffer. The Ecological indicators to capture the effects of fishing on

importance of accounting for environmental impacts (including climate biodiversity and conservation status of marine ecosystems.

change), and predator–prey interactions when considering trade-offs Ecol Ind 2016, 60:947-962.

between fisheries management scenarios is highlighted. Recent ecosystem state and trends over time are analysed for a set of

ecological indicators that is augmented by a complementary set of

9. Costello MJ, Coll M, Danovaro R, Halpin P, Ojaveer H, biodiversity-centered indicators. This is in an attempt to better describe

Miloslavich P: A census of marine biodiversity knowledge, and assess the status of exploited marine ecosystems in a comparative

resources, and future challenges. PLoS ONE 2010, 5:e12110. context.

10. Bolger T: The functional value of species biodiversity: a review. 28. Halpern BS, Longo C, Hardy D, McLeod KL, Samhouri JF,



In and Environment: Proceedings of the Royal Irish Katona SK, Kleisner K, Lester SE, O’leary J, Ranelletti M,

Academy. Royal Irish Academy; 2001:199-224:. December. Rosenberg AA: An index to assess the health and benefits of

the global ocean. Nature 2012, 488:615-620.

11. Christensen V: Managing fisheries involving predator and prey The Ocean Health Index (OHI) comprises a multitude if indicators to

species. Rev Fish Biol Fish 1996, 6:417-442. measure ten key goals that would ensure healthy socio-ecological marine

systems. The OHI is computed for coastal areas all over the globe.

12. Pauly D, Christensen V, Dalsgaard AJ, Froese R, Torres FJ:

Fishing down marine food webs. Science 1998, 279:860-863. 29. Tittensor DP, Walpole M, Hill SL, Boyce DG, Britten GL,

 Burgess ND, Butchart SH, Leadley PW, Regan EC, Alkemade R,

13. Essington TE, Beaudreau AH, Wiedenmann J: Fishing through Baumung R: A mid-term analysis of progress toward

marine food webs. Proc Natl Acad Sci USA 2006, 103:3171-3175. international biodiversity targets. Science 2014, 346:241-244.

55 indicators are identified and underlying data sets scrutinized to assess

14. Swartz W, Sala E, Tracey S, Watson R, Pauly D: The spatial

the progress towards addressing the 20 biodiversity-based ‘Aichi

expansion and of fisheries (1950 to

Targets’. These targets span terrestrial, freshwater and marine ecosys-

present). PLoS ONE 2010, 5:e15143.

tems and suggest that efforts underway will be unlikely to improve

biodiversity by 2020.

15. Morato T, Watson R, Pitcher TJ, Pauly D: Fishing down the deep.

7

Fish Fisheries 2006, :24-34. 30. Coll M, Lotze HK: In Perspectives on Oceans Past: A Handbook of

Marine Environmental History. Edited by Poulsen , Ma´ n˜ ez tle .

16. Christensen V: Fishing down through the food web. Fisheries

Springer; 2016:107-132. vol. in press.

2015, 40:370-372.

31. Shin YJ, Shannon LJ: Using indicators for evaluating,

17. Shannon LJ, Coll M, Bundy A, Gascuel D, Heymans JJ, Kleisner K,

comparing and communicating the ecological status of

 Lynam C, Piroddi C, Tam J, Travers M, Shin YJ: Trophic level-

exploited marine ecosystems. 1. The IndiSeas Project. ICES J

based indicators to track fishing impacts across marine

Marine Sci 2010, 67:686-691.

ecosystems. Marine Ecol Progr Series 2014, 512:115-140.

Trophic-level based indicators derived from survey data, catch data and 32. Shin YJ, Shannon LJ, Bundy A, Coll M, Aydin K, Bez N,

models are examined for effectiveness of capturing the ecosystem Blanchard JL, Borges MF, Diallo I, Diaz E et al.: Using indicators

impacts of fishing. It is important to consider the exploitation history for evaluating, comparing and communicating the ecological

and ecosystem characteristics when interpreting indicator trends. status of exploited marine ecosystems. 2. Setting the scene.

ICES J Marine Sci 2010, 67:692-716.

18. Coll M, Steenbeek J: Standardized ecological indicators to

assess aquatic food webs: the ecoind software plug-in for 33. Bundy A, Coll M, Shannon LJ, Shin YJ: Global assessments of

with ecosim models. Environ Model Softw 2017,  the status of marine exploited ecosystems and their

89:120-130. management: what more is needed? Curr Opin Environ Sustain

2012, 4:1-8.

19. Shannon LJ, Coll M, Neira S: Exploring the dynamics of This paper highlights the worrying position some ecosystems find them-

ecological indicators using food web models fitted to time selves in terms of poor fisheries management, high vulnerability to climate

series of abundance and catch data. Ecol Ind 2009, 9:1078- change effects and heavy ecosystem impacts of fishing. It provides the

1095. context in which the IndiSeas (Indicators for the Seas) programme is

operating to assess ecosystem status using ecological, human dimen-

20. Heymans JJ, Coll M, Libralato S, Morissette L, Christensen V:

sion and climate indicators.

Global patterns in ecological indicators of marine food webs: a

modelling approach. PLoS ONE 2014, 9:e95845. 34. Blanchard J, Coll M, Cotter J, Link J, Trenkel V, Vergnon R,

Yemane D, Shin YJ: Trend analysis of indicators: a comparison

Marine

21. Pinsky ML, Worm B, Fogarty MJ, Sarmiento JL, Levin SA: of recent changes in the status of marine ecosystems around

taxa track local climate velocities 341

. Science 2013, :1239- the world. ICES J Marine Sci 2010, 67:732-744.

1242.

35. Bundy A, Shannon LJ, Rochet MJ, Neira S, Shin YJ, Hill L, Aydin K:

22. Brander K: Improving the reliability of fishery predictions under The Good(ish), the Bad and the Ugly: a tripartite classification

climate change. Curr Clim Change Rep 2015, 1:40-48. of ecosystem trends. ICES J Marine Sci 2010, 67:745-768.

23. Hare JA, Morrison WE, Nelson MW, Stachura MM, Teeters EJ, 36. Fu C, Large S, Knight B, Richardson A, Bundy A, Reygondeau G,

Griffis RB, Alexander MA, Scott JD, Alade L, Bell RJ, Chute AS: A Boldt J, van der Meeren GI, Torres MA, Sobrino I et al.:

vulnerability assessment of fish and invertebrates to climate Relationships among fisheries exploitation, environmental

change on the Northeast US continental shelf. PLoS ONE 2016, conditions, and ecological indicators across a series of

11:e0146756. marine ecosystems. J Marine Syst 2015, 148:101-111.

24. Ben Rais Lasram F, Guilhaumon F, Mouillot D: Fish diversity 37. Bundy A, Chuenpagdee R, Boldt JL, Fatima Borges M,

patterns in the Mediterranean sea: deviations from a mid- Camara ML, Coll M, Diallo I, Fox C, Fulton EA, Gazihan A, Jarre A:

domain model. Marine Ecol Progr Series 2009, 376:253-267. Strong fisheries management and governance positively

Current Opinion in Environmental Sustainability 2017, 29:89–97 www.sciencedirect.com

Assessing changes in marine biodiversity Shannon and Coll 97

impact ecosystem status. Fish Fisheries 2017, 18: 45. Shannon LJ, Osman W, Jarre A: Communicating changes in

412-439. state of the southern Benguela ecosystem using trophic,

model-derived indicators. Marine Ecol Progr Series 2014,

38. Halpern BS, Longo C, Scarborough C, Hardy D, Best BD, 512:217-237.

Doney SC, Katona SK, McLeod KL, Rosenberg AA, Samhouri JF:

Assessing the health of the US west coast with a 46. Osman W: Trophic Model-generated Indicators of the Southern

regional-scale application of the Ocean Health Index. PLoS Benguela Ecosystem for Communicating with Fisheries Managers.

ONE 2014, 9:e98995. University of Cape Town; 2010:154:. Masters dissertation.

39. SCBD (Secretariat of the Convention on Biological Diversity): 47. Lockerbie E, Shannon LJ, Jarre A: The use of ecological, fishing

Global Biodiversity Outlook 3. SCBD, Montreal. Canada. 1. UNEP  and environmental indicators in support of decision making in

World Conservation Monitoring Centre; 2010. Southern Benguela fisheries. Ecol Model 2016, 69:473-487.

A decision-tree framework is developed for assessing the status of the

40. Butchart SHM, Walpole M, Collen B, Van Strien A,

Southern Benguela ecosystem with respect to fishing. Ecological indi-

Scharlemann JPW, Almond REA, Baillie JEM et al.: Global

cator trends (based on the IndiSeas set of indicators) are examined over

biodiversity: indicators of recent declines. Science 2010,

time and considered in the context of environmental indicator trends, to

328:1164-1168.

arrive at a weighted, score-based assessment of ecosystem status.

41. UNEP, CBD: UNEP/CBD/COP/DEC/X/2 2010’. 2010.

48. Lockerbie EM, Coll M, Shannon LJ, Jarre A: The use of indicators

for decision support in northwestern Mediterranean Sea

42. Dı´az S, Demissew S, Carabias J, Joly C, Lonsdale M, Ash N,

fisheries. J Marine Syst 2017, 174:64-77.

Bartuska A: The IPBES Conceptual Framework — connecting

nature and people. Curr Opin Environ Sustain 2015, 14:1-16.

49. Lockerbie EM, Lynam CP, Shannon LJ, Jarre A: Applying a

decision tree framework in support of an ecosystem approach

43. Coll M, Shannon LJ, Yemane D, Link J, Ojaveer H, Neira S,

to fisheries: IndiSeas indicators in the North Sea. ICES J Marine

Jouffre D, Labrosse P, Heymans JJ, Fulton EA, Shin YJ: Ranking

Sci 2017 http://dx.doi.org/10.1093/icesjms/fsx215.

the ecological relative status of exploited marine ecosystems.

ICES J Marine Sci 2010, 67:769-786.

50. Burgass MJ, Halpern BS, Nicholson E, Milner-Gulland EJ:

Navigating uncertainty in environmental composite

44. Rochet MJ, Trenkel V, Bellail R, Coppin F, Le Pape O, Mahe´ JC,

indicators. Ecol Ind 2017, 75:268-278.

Morin J, Poulard JC, Schlaich I, Souplet A, Ve´ rin Y: Combining

indicator trends to assess ongoing changes in exploited fish

51. Geijzendorffer Ilse, et al. this issue.

communities: diagnostic of communities off the coasts of

France. ICES J Marine Sci 2005, 62:1647-1664. 52. Balvanera Patricia, this issue.

www.sciencedirect.com Current Opinion in Environmental Sustainability 2017, 29:89–97