Evaluating Fisheries Management from a Life Cycle Perspective with New Approaches to By-Catch Impacts

Evaluating fisheries management from a Life Cycle perspective with new approaches to by-catch impacts

Sara Hornborg

Licentiate thesis

Keywords: LCA, fisheries management, red listed fish species, trophic indicators

Sustainable Food Production, Swedish Institute for Food and Biotechnology (SIK)

Department of Biological and Environmental Sciences, University of Gothenburg, Sweden

Printed by Kompendiet, Aidla Traiding AB, Gothenburg, Sweden 2012

ISBN: 91-89677-50-1

The licentiate seminar will be held at 10.00 on the 26th of April, 2012, at the Department of Biological and Environmental Sciences in Gothenburg (Botan, Carl Skottsbergs gata 22).

External reviewer: PhD Henrik Österblom, Stockholm Resilience Center, Stockholm University

Supervisors: PhD Friederike Ziegler (main), Sustainable Food Production, the Swedish Institute for Food and Biotechnology (SIK)

Assoc. Prof. Per Nilsson, Department of Biology and Environmental Sciences, University of Gothenburg

PhD Daniel Valentinsson, Department of Aquatic Resources, Swedish University of Agricultural Sciences, Lysekil

Examiner: Professor Kristina Sundbäck, Department of Biology and Environmental Sciences, University of Gothenburg

Till mina älskade barn Elias och Ella

För Framtida Fina Fiskpinnar

Abstract

Life cycle assessment (LCA) couple resource use and environmental impacts attributed to a product during its life cycle. Method development is still needed to better quantify (in the case of seafood) impacts on target stock, by-catch and seafloor disturbance. The present thesis focuses on improved assessment of unintentional catches in LCA, and suggests two complementary methods to assess their impacts: primary production required (PPR, in mass of carbon accumulated per kilo wet weight of a species at a certain trophic level) and the amount of red listed fish species (VEC, in mass or number) in discards per kilo of seafood product.

Based from the results from studying Swedish fisheries landings in comparison to survey data, onboard monitoring of discards and data on primary production from the Kattegat and Skagerrak during the last century, quantifying PPR from discards is suggested as a differentiated seafood product impact. Different gears and targeting patterns varied greatly in terms of PPR from the discarded part of the catch, additionally shown for the mean trophic level (MTL) of catch, landing and discard. Even if this show that different seafood products can be attributed different PPR, the interpretation in terms of impact from having different PPR values must be made with caution. PPR must be placed in a historical context, as well as it is necessary with complementing information on impact on depleted stocks, susceptible to further impacts from discards.

As it was additionally found that the Swedish national IUCN red list of marine fish species showed high consistency with scientific advice, as well as sensitive life history traits, quantifying the amount of threatened fish species in discards (VEC) showed to be an appealing complementing indicator for the sensitivity of different discard compositions. In discard data from the demersal trawl fisheries in the Kattegat and Skagerrak, differences in amount of VEC per kilo of landing were found between fleet segments targeting different species. By this, it is suggested that VEC could be used as a carrier of aggregated information of the susceptibility of the impact to be included within the LCA framework.

The resource use and environmental impacts of a seafood product is strongly linked to fisheries management (e.g. gear regulations, effort restrictions and quotas), as prior LCA‘s of capture fisheries have been found to in general be dominated by the fishing phase. By using a life cycle approach to the management of the Norway lobster (Nephrops norvegicus) trawl fisheries in the Kattegat and Skagerrak area, LCA was tested as a new tool to optimize marine resource use in a broader perspective. With the new approaches to discard assessment applied, it was found that from a product perspective, protecting locally depleted fish stocks in the area comes with a trade-off in e.g. seafloor area swept and fuel use. Fisheries management needs to consider that both fish and fossil fuel resources are presently scarce, which makes an integrated perspective of increasing importance to create an overall sustainable resource use.

In the case study, it was additionally found that assessing discards in LCA by combining PPR and VEC, enhance the picture of varied discard impact depending on species composition. Still, further method development is needed regarding impacts on target stocks and differentiated seafloor impacts.

Svensk sammanfattning

Hur kan man koppla en fisk- och skaldjursprodukt till dess breda miljöpåverkan och använda denna information för till exempel produktrelaterad information? Ett sätt är att använda livscykelanalys (LCA), en metod som beräknar allt resursutnyttjande och all miljöpåverkan längs med en produkts livscykel, ofta i ett ‖vaggan-till-graven-perspektiv‖. På så vis kan man jämföra olika produkters miljöpåverkan, som skillnader mellan t.ex. glas- och plastflaskor, växthusodlade och frilandsodlade grönsaker; eller identifiera förbättringspotentialer inom produktionsprocess som skillnader mellan olika fodersammansättningar inom laxodling.

Eftersom LCA som metod är relativt ny har den brister vad gäller att inkludera biologisk miljöpåverkan, och fokus har oftast varit på bränslebehovet. Tidigare livscykelanalyser av fisk- och skaldjursprodukter har visat att miljöavtrycket varierar stort mellan olika fångstmetoder inom fisket. För att dock kunna genomföra en så heltäckande utvärdering av fiskets miljöpåverkan som möjligt behövs metodutveckling, för fisk- och skaldjursprodukter främst för påverkan av målart, bifångster och bottenyta.

Fiskets miljöpåverkan genom oönskade fångster föreslås att skattats på två olika sätt: antalet hotade fiskar (rödlistade) och det s.k. primärproduktionsbehovet (ackumulerad mängdenergi som behövts för att producera ett kilo av en art beroende på placering i näringskedjan) i den del av fångsten som kastas i relation det som säljs (landas). Dessa två metoder testas i en fallstudie av svensk trålning efter havskräfta (studie I) samt diskuteras i två separata mer metodinriktade studier (II & III).

Användning av trofiska mätpunkter inom fisket (studie III)

Fisket påverkar näringsväven i havet, där topprovdjur generellt har varit hårt drabbade. En vetenskaplig debatt om hur man bäst kan beskriva denna påverkan har pågått länge. Som ett mått på utarmningen av rovfiskar har medeltrofinivån i fisket föreslagits vara ett mått på fiskets uthållighet. Utarmningen kan även ses ur ett resursperspektiv, eftersom det innebär en högre energikostnad att producera ett kilo av en art på en högre plats i näringskedjan (på grund av de stora näringsförlusterna mellan varje nivå). Primärproduktionsbehovet per landning kan därmed anses vara valutan som visar på skillnaden mellan olika typer av fiske. Det nuvarande fiskets behov i relation till tillgänglig produktion verkar i ett globalt perspektiv dessutom vara större än vad som skulle känneteckna ett långsiktigt hållbart resursutnyttjande.

I studie III utvärderades svensk landningsdata från Kattegatt och Skagerrak under det senaste århundradet vad gäller medeltrofinivå och primärproduktionsbehov. Resultatet jämfördes med data från provfiske och högupplöst data som även inkluderade den bortkastade delen av fångsten i ett antal trålfisken längs västkusten, samt halter av primärproduktion. Studien visar att redskapsanvändning och fiskeinriktning markant påverkar båda dessa indikatorer, och att det var viktigt att titta även på den kastade delen av fångsten. Blandtrålsfiske efter fisk och kräfta kan till exempel ha enbart fem procent av sitt totala primärproduktionsbehov från den landade delen av fångsten, medan renare bottentrålsfiske efter fisk har motsvarande över åttio procent. Detta gör indikatorerna lämpliga för att utvärdera skillnader i påverkan mellan olika fiskemetoder inom ett område och över tid, speciellt genom att titta på den bortkastade delen,

5 och mindre lämplig på global nivå. Det är dock viktigt att känna till områdets historia för att kunna säga något om skadepotential, speciellt för fiskets primärproduktionsbehov som visade sig ha minskat över tid i förhållande till tillgänglig primärproduktion, samt komplettera informationen med uppgifter om påverkan av överexploaterade fiskbestånd.

Rödlistade fiskarter som indikatorer för påverkan från oönskad fångst (studie II)

Hoten mot rödlistade fiskarter är ofta starkt kopplade till överexploatering genom fiske. De arter som historiskt har fått mest uppmärksamhet som bifångst är marina däggdjur, fåglar och sköldpaddor, medan uppmärksamheten är generellt lägre kring fiskarter med samma hotbild.

I studie II utvärderades den svenska rödlistningen av fiskar i relation till förvaltningens rådgivning samt till egenskaper hos fisk som är känsliga för fisketryck (stor maxlängd, hög maxålder och hög ålder vid könsmognad). Rödlistans klassificering av fiskar i Sverige visade sig stämma väl överens med de övriga skattningar av känslighet för fisketryck som testades i studien. Genom att studera mängd eller massa rödlistade fiskarter i den kastade delen av fångsten i förhållande till den använda delen visade det sig att denna andel skiljer sig mellan olika typer av redskap i området. Utöver icke hotade arter, kastade blandtrålsfisket inriktat mot havskräfta störst andel hotade fiskarter per landat kilo, runt trettio exemplar för varje tio landade kilon, medan artselektiv trålning efter räka endast genererade en hotad fiskart kastad per tio kilo landning. Som LCA-tillämpning för att skatta oönskade fångsters påverkan av känsliga arter från en fisk- eller skaldjursprodukt, föreslås därmed att skatta hur mycket rödlistade fiskar som kastas bort i förhållande till varje kilo som tas iland. Denna information kan ses som en sammanvägd bild av känsliga egenskaper och grad av överfiske.

Utvärdering av förvaltningen av trålfisket efter havskräfta i Sverige (studie I)

Bottentrålsfisket på västkusten, som tidigare har varit ett blandat fiske efter fisk- och skaldjur, är i dagsläget starkt begränsat av EU:s återuppbyggnadsplaner för torsk. Införandet av en selektiv trål (som sållar bort många fiskarter), har varit nödvändig för att kunna fortsätta fiska havskräfta, något som alltmer har lett utvecklingen mot en-artsfisken. Genom att med ett livscykelanalys-perspektiv studera miljöpåverkan och resursförbrukning ur ett bredare produktperspektiv som kan kopplas till ett kilo fisk- och skaldjur från vanlig trål jämfört med en selektiv trål kan man lättare se vilka omedvetna avvägningar som gjorts vid förvaltningsbeslut och därmed skapa ett mer integrerat beslutsunderlag. Studie I beräknade kastad fångst (mängd, primärproduktion och hotade arter), bottenyta påverkad, bränsleförbrukning & växthusgasutsläpp för att landa ett kilo fisk- och skaldjur med selektiv respektive vanlig bottentrål i Kattegatt respektive Skagerrak. Dataunderlag som användes var ett års (2009) loggbok (redskap, tråltimmar, landningar, fiskebåtarnas kW) och provtagen data över den kastade delen av fångsten under samma år. Bränsleförbrukning och bottenyta beräknades med hjälp av modeller och uppgifter från loggboken.

Studien visar att miljöpåverkan från trålning efter havskräfta varierar stort beroende på redskap och område. Artselektiv bottentrålning efter havskräfta skyddar kraftigt överfiskade fiskbestånd, men på bekostnad av ökat bränslebehov (och därmed ökade utsläpp av växthusgaser). Det ger också en större bottenyta påverkad per kilo landning. Genom denna

6 sammanvägda bild av miljöpåverkan från ett förvaltningsbeslut får man ett mer integrerat underlag kring aspekter som vid beslutsfattandet låg utanför förvaltningens direkta åtagande. Följaktligen uppstår en motsättning mellan en förvaltningsåtgärd för att skydda lokala torskbestånd och det globala perspektivet, eftersom åtgärden medför ett ökat behov av fossila bränslen och ökade växthusgasutsläpp per kilo landning.

Slutsatser

Genom att bättre kunna skatta påverkan från att kasta en del av fångsten kan man med miljösystemanalys som LCA bättre undvika att bortse ifrån viktiga aspekter av miljöpåverkan på grund av avsaknad av metod. Primärproduktionsbehovet belyser en viktig aspekt, men säger ingenting om huruvida en påverkad art är vanlig, sällsynt, ökar eller minskar. Förekomsten av hotade arter säger å andra sidan ingenting om resursbehovet. En kombination av skattning av båda två i den oönskade delen av fångsten ger en mer initierad bild av miljöpåverkan från den bortkastade delen av fångsten. På så sätt ges möjligheter till mer heltäckande produktrelaterad information samt bredare utvärderingar av fiskeriförvaltning för att skapa ett mer integrerat underlag för beslutsfattning för ett mer hållbart resursutnyttjande. Fortsatt metodutveckling för att inkludera påverkan på målart och botten rekommenderas för att ytterligare stärka LCA som förvaltningsverktyg och möjliggöra jämförelser mellan olika fisk- och skaldjursprodukters bredare miljöpåverkan.

Acknowledgements

First, I am of course greatly in debt to my knowledgeable and overall fantastic supervisors. Friederike, your sharp brain does not miss a thing and you are always extremely supporting and encouraging! Daniel and Per, your long experiences from fisheries management and conservation planning have contributed to many extremely interesting discussions and insights.

I would also like to thank my co-PhD-colleague Andreas Emanuelsson, for interesting discussions and supporting words. Also, the rest of our project group, Leif Pihl (GU) and Mattias Sköld (SLU), it is always a treat when we all get together. The same goes for my department at SIK, Sustainable Food Production, for hearty and inspiring coffee breaks, sustainable food production can never be a boring topic! Cheila (Portuguese ―sardine- hugger‖) and Veronica (miss Eco-label), extra dear colleagues in the field of sustainable seafood!

Katja Ringdahl for providing and assisting with data, not to mention all the patience with all the questions that I have had! Mikael Svensson at ArtDatabanken, for interesting discussions and invaluable data. Andrea Belgrano and Valerio Bartolino, for discussing and commenting on paper III. Kristina Sundbäck, thank you for taking care of all practicalities in the role of examiner.

All friends in Göteborg that have lightened up the little spare-time I have had in recent years: Malin, Mia, Robin, Tea, Björn, Lena, Lars, Sara, and more…and all others up the west coast (Erica, Andreas, Malin K, Håkan, Kalle, Marie, Fredrik…) even if a quick car ride outside town has been sadly rare in recent years, it is always great when we meet. Thank you all for support and inspiration!

Last, but certainly not least, my little family with my ever supporting husband Totte, ―up-and- coming-marine-biologist‖ -Elias and ―ever-happy-and-full-of-jokes‖ -Ella. Linnéa, for helping me keeping it all together and keeping me in contact with the world outside fisheries, such as the latest music and fashion (and for taking care of my physical training ). You all form the base to my existence.

Thank you all!

Sara

The thesis is based on the following list of papers:

Paper I Hornborg, S., Nilsson, P., Valentinsson, D. & Ziegler, F. Integrated environmental assessment of fisheries management: Swedish Nephrops trawl fisheries evaluated using a lifecycle approach. Marine Policy (2012) http://dx.doi.org/10.1016/j.marpol.2012.02.017

In press. Reprinted with kind permission, copyright of Elsevier.

Paper II Hornborg, S., Svensson, M., Nilsson, P. & Ziegler, F. Use of red listed fish species as indicators for fishing by-catch impact on sensitive species. Manuscript

Paper III Hornborg, S., Belgrano, A., Bartolino, V., Valentinsson, D. & Ziegler, F. Mean Trophic Level and Primary Production Required in Swedish fisheries over a century: prospects and limitations of the indicators. Manuscript

Table of contents

Definitions and abbreviations

1. Aim 2. Methods and data used

2.1Methods

2.2 Data

3. Introduction 4. Life Cycle Assessment and seafood production

4.1 General LCA methodology

4.2 LCA of capture fisheries

4.3 Fuel use in Swedish Nephrops trawl fisheries

5. Environmental impacts of capture fisheries

5.1 Target catch

5.2 Unintentional catches: By-catch and discard

5.2.1 Non-commercial species in discards

5.2.2 Discard of commercial species

5.3 Benthic impacts

6. New approaches to by-catch assessments

6.1 Threatened species

6.2 Food web interactions

7. Fisheries management and LCA 8. Conclusions and future outlook

References

Paper I

Paper II

Paper III

Definitions and abbreviations

By-catch The part of the catch that is not directly targeted consisting of two parts: one that is utilized, but most lack sufficient management due to data deficiency; one that is discarded at sea, could be undersized, quota filled species or non-commercial species, not recorded in logbooks.

Discard The part of the catch in a fishery that is thrown away at sea and only recorded in onboard monitoring programs. This could be non-commercial fish- and invertebrate species, but also juveniles of target species, quota restricted marketable species or marketable species with lower economic value that the fishing preference (high-grading).

CBD Convention of Biological Diversity

CPUE Catch per unit effort

CITES Convention on International Trade in Endangered Species of Wild Fauna and Flora

EBFM Ecosystem Based Fisheries Management

GHG Greenhouse Gas

HCFC/HFC Hydrochlorofluorocarbon/ Hydrofluorocarbons (freons)

ICES International Council for the Exploration of the Sea, scientific community with participants from all states bordering the North Atlantic and the Baltic Sea.

―… co-ordinates and promotes marine research on oceanography, the marine environment, the marine ecosystem, and on living marine resources in the North Atlantic.”

IPCC Intergovernmental Panel on Climate Change

IUCN International Union for Conservation of Nature

Landings The part of the catch that is recorded in logbooks and brought to market.

LCA Life cycle assessment

MTL Mean trophic level

PPR Primary production required

RLI Red list index

TAC Total Allowable Catch, the maximum allowed amount of a certain stock to be landed per year. The concept is confounding as it is not referring to catch, but landing, i.e. not including discards.

TE Transfer efficiency

TL Trophic level

VEC Vulnerable, Endangered or Critically Endangered (according to IUCN criteria)

1. Aim

The aim of this thesis is two-fold:

 To establish a framework for assessing important biological impacts from unintentional catches in capture fisheries for use in e.g. Life Cycle Assessment (LCA) studies.  Use the expanded LCA as a tool for evaluation of the broader environmental impacts of decisions in fisheries management.

2. Methods and data used

2.1 Methods

Life cycle assessment (LCA) is a method to couple all resource use and environmental impacts of relevance to an entity of focus, a functional unit, often with a ―cradle-to-the- grave‖-perspective. In paper I, a form of LCA called ―life cycle thinking‖ was used to study the most important phase in the lifecycle of a seafood, the fishing phase, in order to assess the importance of fisheries management for the outcome of a product from capture fisheries, as well as testing new approaches to assess potential impacts from by-catch within the LCA framework. The functional unit of the study was one kg of mixed landed seafood from the Swedish Norway lobster (Nephrops norvegicus) trawl fishery, in terms of mean values for one year (2009). Impacts considered were discards (total mass, juveniles of target stock, primary production required and threatened species affected); seafloor area swept; fuel use and greenhouse gas emissions; and a qualitative discussion about the impact on the target stock. Important to note is that the impacts are only considered at the level of ―potential to cause impact‖, not ―effect‖.

In paper II, the consistency of the red listing of marine fish species in Sweden (with guidelines provided by the International Union for Conservation of Nature (IUCN) at iucnredlist.org) was assessed in relation to scientific advice on stock status and data on life history traits that have prior been found to indicate sensitivity to fishing pressure. The amount of threatened fish species (individuals, mass and number of species) was further studied in the discard composition of demersal trawl segments in the Kattegat and Skagerrak area. The intent with this study was to evaluate the robustness and possibilities of using red listed fish species in discards as indicators for the seafood product‘s impact on sensitive and overexploited fish species, to be used for communication (e.g. LCA) and fisheries management evaluation.

In paper III, estimates on primary production required (PPR; model from Pauly & Christensen, 1995) as well as mean trophic level (MTL; model from Pauly et al., 1998) of landings, catch, discard and survey data from the Kattegat and Skagerrak was made. As trophic indicators are at present used in several disciplines, the approach in this paper was to contribute to the understanding of limitations, as well as possibilities, of using the indicators for various purposes.

2.2 Data

The data used for all three studies were:

 Swedish fisheries landings during1903-2010 (available at www.ices.dk)  Survey data from the 1970s from the International Bottom Trawl Survey (IBTS) co- ordinated by the International Council for Exploitation of the Seas (ICES) and available at www.ices.dk.  Data on discards for one year (2009; 167 hauls) from sampling by trained scientific observers from the Department of Aquatic Resources (Institute of Marine Research, Swedish University of Agricultural Sciences) in accordance with the Data Collection Framework (DCF; EC Council Reg 199/2008).  Primary production data came from the Swedish Meteorological and Hydrological Institute (www.smhi.se), sampled during 1985-2010.  Fuel use was based on a model derived from Danish fisheries by Bastardie et al. (2010) which was applied on Swedish logbook data from one year (2009) on effort, kW and landings; adjusted from interviews with fishermen in the studied segments (12 boats landing approximately 25% of the Nephrops trawl landings).  Life history traits and threat status was provided by the Swedish Species Information Centre (ArtDatabanken,www. slu.se).  Scientific advice on stock status was taken from ICES (www.ices.dk).  Trophic level of fish species was taken from www.fishbase.org; trophic level of invertebrates from www.seaaroundus.org.  Combustion figures for greenhouse gas emissions from diesel use came from Swedish Petroleum & Biofuel Institute (www.spbi.se)  Area impacted by trawl was based on a model derived from a study in the same area in Nilsson & Ziegler (2007) and applied on one year (2009) of logbook data on effort, trawl type and landings.

3. Introduction

The history of marine resource use is a sad story (Roberts, 2007). It is easily forgotten what the diversity and size of fish used to be (Jackson, 2001), as former abundances are increasingly distant and we now only have pictures left to be amazed at (Pauly, 1995; McClenachan, 2009). Former exploitation patterns, as well as its effects, can also be seen in statistics, such as the Swedish landings of Atlantic Bluefin tuna (Thynnus thunnus) that appeared in landing statistics in the Kattegat and Skagerrak area in the 1930s (Figure 1).

Figure 1. Swedish landings of Bluefin tuna (Thynnus thunnus) in the Kattegat and Skagerrak area. Data for the 60s and early 70s are missing due to landings being aggregated with the North Sea. The last landing was 1 ton in 1991.

Bluefin tuna was before this regional depletion an ecologically important top predator in the North Sea ecosystem for 2-3 months per year (MacKenzie & Myers, 2007). The history of exploitation of this species is only one in the line of repeated local depletions of stocks (Jackson et al., 2001). In fact, the last century‘s increase in global landings has only been enabled from expansion of fishing grounds, with the greatest expansion during the 1980s- early 1990s, followed by a decline of newly exploited areas coinciding with a decline in global fish landings (Watson & Pauly, 2001; Swartz et al. 2010).

To mitigate the negative effects from the competitive nature of fisheries, management of fisheries has evolved. Politicians set quotas based on scientific advice after undergoing a political negotiation process between countries with interests in the fishery. This protection of marine resources by governmental authorities took off quite late in the history of fisheries exploitation, with Beverton and Holt (1957) providing the initial fundamental theory for optimum resource use. Their models have been heavily debated since then, revisited and revised (Larkin, 1977; Mace, 2001).

Management of a natural resource is not straightforward. The definition of success and failure of fisheries management can be seen from different perspectives. The ideal resource use would be to have the highest maximum long-term output of fish production to human use without causing adverse effect on ecosystem structure and functioning, provided this at all can be defined. In reality, politics (i.e. economics) have played a major role, resulting in single species overexploitation and less respect to ecological consequences (MacKenzie & Myers,

2007) or the scientific advice (Cardinale & Svedäng, 2008). The somewhat narrow focus of fisheries managers, has in general failed to acknowledge the complexity of natural resource use and the interactions of several disciplines such as biology, economics and sociology (Browman & Stergiou, 2004; Degnbol et al., 2006), further complicated by insufficient data reporting (Agnew et al., 2009; Zeller et al., 2009).

With anthropogenically driven climate change from combustion of fossil fuels is now established (Solomon et al., 2009) as well as increasing evidence of peak oil having been passed (Aleklett, 2010), it is important to put energy use in fisheries further up on the agenda, especially due to the energy intensity in many fisheries (Tyedmers et al., 2005; Ziegler, 2006; Thrane, 2006; Iribarren et al., 2010) and important interactions between climate change and production of seafood (Rice et al., 2011). Dependency on cheap fossil fuel and greenhouse gas emissions from the fishing fleet cannot be neglected for much longer, but how could it be integrated side by side with other fisheries management considerations?

Meanwhile, the global trend of fish consumption per capita is increasing (FAO, 2010). With health policies promoting increased fish consumption, optimizing marine capture production is increasingly essential (Brunner et al., 2009). As a response to the noticeable failures of management, increased consumer awareness has evolved which create incentives for eco- labeling of seafood products (FAO, 2010). Eco-labeling offers easy-to-grasp information to the consumer saying ―good‖ and has shown to have led to some environmental improvements (MSC, 2011a) even though the same certification systems have been subjected to critique (Jaquet et al., 2010). Unfortunately, eco-labels do not normally consider energy use in the labeling scheme (Thrane et al., 2009), even if there are examples of labels have included this aspect, such as the Swedish KRAV label (krav.se).

Unfortunately, energy use of fisheries is one area of concern that still falls out of scope when setting management priorities (Tydmers et al., 2005). With present fisheries not only described by overexploitation of many commercially valuable fish stocks (Myers & Worm, 2003; FAO, 2010) and wasteful discards (Kelleher, 2005; Catchpole et al., 2005), but also as an industry heavily depending on fuel subsidies (Sumaila et al., 2008), more integrated approaches are needed for future fisheries development (Pauly et al., 2002).

Altogether, there is a societal need for the scientific community to search for robust and quantitative indicators for monitoring, communication and assessing or adjusting fishing policies to secure future fisheries in terms of food security (Cury & Christensen, 2005; Garcia & Rosenberg, 2010). Life cycle assessment (LCA) offers a transparent and integrated methodology to quantify all environmental impacts of relevance coupled to a certain product, with the aim to provide a broader perspective and identify hot spots and improvement potentials often from a cradle-to-grave perspective (ISO 2006a; 2006b). Environmental systems analysis methods, such as LCA, are further recommended to form the base for eco- labeling schemes (ISO 2006c). Could this tool for decision support be the panacea for fisheries management and the development towards an overall sustainable marine resource use?

4. Life Cycle Assessment and seafood production

4.1 General LCA methodology

Life cycle assessment (LCA) consists of four stages, however with an important iterative evaluation of the result from choices made in previous stages:

Goal & scope Definition of the aim of the study, system boundaries such as which processes to include; the object of study (functional unit); choice of impacts to be studied; and other technical aspects such as allocation procedure, i.e. deciding on how to share environmental impacts in multiple outputs.

Inventory The most time consuming part, where data on all resource use and emissions defined in goal and scope are collected and quantified in relation to the functional unit.

Impact assessment All resource use and emissions inventoried are grouped into chosen impact categories and weighted together based on their relative impact contribution potential. For example, GHG emissions are weighted according to IPCC standards.

Interpretation of results The sensitivity of the results from different inputs is, possibly resulting in changes of earlier choices made.

Defining the entity of focus, called the functional unit, is made in the goal and scope. This unit is studied in terms of resource use and environmental impacts, possible along the whole production and distribution line, life time and end of life, depending on the objective of the LCA. As many processes have a multiple output of products, various strategies for distributing the proportional environmental impact and resource use between the different products have been developed, called allocation. Preferably, according to the ISO standard this should if possible be avoided by increasing the level of detail (sub-dividing the system) or system expansion (using an alternative production system for one of the co-products). Otherwise this can be based on physical causal relationships between in and outputs based on e.g. the relative mass, energy or protein content of the co-products, or as the last alternative, based on other relationships (such as their relative economic value). In fisheries, this applies mainly to two situations: when several species are landed together and in processing of fish into various edible products as well as non-edible parts. There are different views on which allocation method is the most accurate for seafood production systems (see e.g. Ayer et al., 2007; Pelletier et al., 2011a), but it is important to remember that the choices made affect the absolute results and this complicates comparisons of results from different LCAs.

4.2 LCA of capture fisheries

In general, prior life cycle assessments of food products have concluded that the early life cycle stage, that is e.g. agriculture or fishing, has the dominating contribution in terms greenhouse gas emissions (GHG) and energy use per final product (Sonesson et al., 2010; Pelletier et al., 2011b). Vegetables are found in the lower range, whereas meat, especially beef, is found in the upper range. Seafood from capture fisheries exhibits broad values of GHG emissions, mainly attributed by fossil fuel use by the fishing vessel. The second important contribution to the GHG emissions from seafood production is possible leakage of refrigerants from cooling equipment on the vessels, if HCFC/HFCs are still in use (Winther et al., 2012). In agricultural based systems, other GHGs of non-fossil origin (biogenic) are more important, such as methane and nitrous oxides.

LCA‘s of seafood production systems began in the early 2000s and have since then attracted increasing interest. As the method is young, methodological development is still needed (Pelletier et al., 2007), e.g. assessing impacts that are more complex to quantify, such as impacts on biodiversity (Curran et al., 2010). Due to lack of methods, focus has been on energy use and GHGs, and these assessments have brought some valuable identification of hot spots between different production systems (e.g. Winther et al., 2012; Vázquez-Rowe et al., 2010). There is however a risk of missing out in providing the comprehensive environmental perspective intended with the method by not having all necessary tools, for example assessing important components of a seafood product such as stock status, biodiversity effects and others with the same quantitative and integrated approach. It has been suggested that energy intensity could act as an indicator for other environmental impacts (Ziegler, 2006; Thrane, 2006), as there is a correlation between stock status and fishing method such as a depleted stock needs more fuel per kilo to land, due to e.g. lower landing per unit effort combined with longer distance to fishing ground (Hospido & Tyedmers, 2005).

A study confirming the energy need correlation to biological impacts is a LCA on Norway lobster (Nephrops norvegicus) caught with creel versus demersal trawl, were fisheries specific impacts new to the LCA framework were included (Ziegler & Valentinsson, 2008). Both swept seafloor area, discard amount and fuel use was found to be considerably higher for trawled Nephrops compared to creel caught ones. However, these findings were complemented with a study focusing on the Nephrops trawl fishery in the area, where the methodological framework for assessing impacts from discards was further expanded (paper I). Without differentiating impacts imposed from discards in terms of new approaches (such as quantifying the vulnerability of discarded fish species and the extra primary production required from discards), conventional trawling would come out as clearly superior to selective trawling as the greenhouse gas emissions are lower per kilo of landing. Even the total discard ratio was shown to be lower. However, by increasing the level of detail and distinguish between possible discard impacts, e.g. selective trawling have discards consisting mainly of less sensitive species (such as juvenile Nephrops) trade-offs in terms of discard impact and fuel efficiency can better be visualized.

4.3 Fuel use in Swedish Nephrops trawl fisheries

Fuel use, GHG emissions and biological impacts in former LCA‘s on Nephrops are summarized in Table 1. Note that the figures are not directly comparable between the studies, as there are differences in goal and scope, importantly the choice of allocation method. Instead, it is attempted to illustrate how different methodological choices affect the absolute results in the studies.

Assessments of the Swedish Nephrops fishery has been done by Ziegler & Valentinsson (2008), Hornborg et al. (paper I) and Ziegler & Hornborg (in prep). The first study used fuel data from 19 questionnaires (of which seven were trawlers). The second study (paper I) applied a fuel model from a Danish study (Bastardie et al., 2010) on Swedish logbook data from 2009, accounting for differences in kW of the boats in the fishery. Based on interviews with fishermen, the model was adjusted to use 40% of kW. Transport assumptions were made regarding the length and speed of steaming to and from fishing ground, resulting in mean values for fuel consumption per landing based on all hauls during one year. The 40 % kW usage have later been found to possibly have been a bit optimistic, when the third study was made possible due to official release of aggregated data for 2009 in the Annual Economic Report on the European fishing fleet by the Joint Research Centre (JRC) of the European Commission (Anderson, J., et al., 2011; Ziegler & Hornborg, in prep). These results are sprung from a top-down approach, using data on the total fuel use by different fleet segments estimated from survey data collected by the Swedish Board of Fisheries. Allocating the total fuel consumption first by trawl hours (assuming that all demersal trawls have approximately the same fuel consumption within a size segment) and then by landing per hour from Swedish logbook data (effort and landings for different gears), an estimated fuel need per landing was obtained. From these results, it was found that approximately 80 % kW effect (if applied to all demersal trawl segments) would be more in line with the total fuel consumption for the fleets according to JRC. However, the lower results in (paper I) could also have been affected by the transportation scenarios chosen. It could also be that the estimates in the Annual Economic Report could be somewhat high. The fuel data in Sweden are unfortunately highly classified information, allowing raw data for independent research would have provided better starting point for all LCA studies on fuel use in fisheries, aiming to contribute important and integrated information to stakeholders, managers and the industry itself.

According to the Swedish Board of Fisheries, fuel use per kilo landing was in 2007 in the range of 2.5-3.8 l/kg for Nephrops trawling and 0.9-0.3 l/kg for mixed demersal trawling depending on boat size (Bengtsberg, 2007). However, the gear and boat definitions in this report was somewhat different than in Hornborg et al., (paper I), e.g. no separation between different selectivity of gears was made. In addition, both landings and fuel use differ between years, with possible effect on the fuel use per kilo seafood product (Ramos et al., 2011).

Table 1. Main LCA results from earlier studies including Nephrops fisheries. Important to note that the figures are not directly comparable as there are differences in goal and scope between the studies (with particular effects from using different allocation methods of attributing impacts per species in mixed fisheries). Discardjuv refers to Nephrops.

Gear Year Country Diesel GHG Discard Seafloor Discardjuv VEC PPRdisc Reference 2 (data) (liters) (CO2e) (kg) (m ) (kg) (No.) (kg C)

Mixed trawl Denmark 1 Tyedmers, 20041 Mixed trawl Denmark 6 Thrane 20042 Mixed trawl 4 Thrane 20063 Mixed trawl 2004 Sweden 9 27.8 4.5 33 000 Ziegler & Valentinsson (2008)3 Selective trawl 2004 Sweden 1.4 Ziegler & Valentinsson (2008)3 Creel 2004 Sweden 2.2 7.2 0.4 1.6 Ziegler & Valentinsson (2008)3 Mixed trawl Spain 25.5 Iribarren et al. (2010)4 Mixed trawl 2009 Sweden (Kattegat) 1.8 5.5 1.7 15 000 0.8 2.7 89 Hornborg et al. (paper I)1 Mixed trawl 2009 Sweden (Skagerrak) 1.3 3.8 1.2 10 000 0.2 3.2 120 Hornborg et al. (paper I)1 Selective trawl 2009 Sweden (Kattegat) 2.4 6.8 2.5 22 000 0.8 1 88 Hornborg et al. (paper I)1 Selective trawl 2009 Sweden (Skagerrak) 2.4 7.0 1.3 17 000 0.7 0.5 31 Hornborg et al. (paper I)1 Selective trawl 2002- Sweden 3.4-8.8 Ziegler & Hornborg (in prep)4 2009 Mixed trawl 2002- Sweden 0.5-1.6 Ziegler & Hornborg (in prep)4 2009

1 Mass allocation 2 System expansion 3 Economic allocation 4 Mass allocation. The range illustrates different size classes of boats, with the lowest values attributed to the smallest boats (data from 2009). 20

5. Environmental impacts of capture fisheries

It must be noted that a range of scientific disciplines must be involved if to be conclusive on which categories of environmental impacts are of concern from marine capture fisheries and many with synergetic effects (Rogers et al., 2011; Noone et al., 2012). Many impacts are of concern to ecosystem functioning, which so far only have found to be highly complex and impossible to fully grasp in the marine environment (Stachowicz et al., 2007). Not surprisingly, whereas it has been repeatedly documented that fisheries in the longer perspective have impacts on biodiversity (e.g. McClenachan, 2009), the exact cause-effect chain leading to altered function and resilience, is not clearly established (Worm & Duffy, 2003; Duffy et al., 2007). Identifying which interactions that have the potential to affect the resilience of the ecosystem, not to mention quantifying the potential impacts, is unlikely to fully be possible to incorporate within a framework such as LCA or any other form of assessment at present level of understanding.

Identifying all biotic impacts important to consider in order to have a non-excluding approach of the LCA framework is therefore difficult, but a general rule of thumb could be target stock impacts, unintentional catches and seafloor disturbance. Within these three categories, there are several diversified impacts, as well as interactions within and between them. Further unwanted impacts from fisheries, besides these general issues are certainly of concern, such as interaction with seabirds (Cury et al., 2011). This thesis will not cover all areas of concern, but focus on indicators that could be used to assess different potential impacts from unintentional catches.

5.1 Target catch

The most obvious impact of marine capture fisheries at present would be removal of biomass that has led to stock depletion due to overexploitation (Jackson et al., 2001). Fish species formerly common on our dinner plates, and to some extent still are, have ended up on lists of species threatened with extinction (IUCN, 2011).

As a food production system, capture fisheries production depends to a greater extent on natural replenishment, i.e. ecosystem functioning, in comparison to most other types of food items, which rely on the intensified and more man controlled production systems of agriculture. This is important, as agricultural systems have brought on vast land transformations, with great effects on pristine diversity and ecosystem functioning (Foley et al., 2011); but while the agricultural landscape is now at times considered to be esthetically pleasing, even worth protection for cultural reasons, exploitation of the sea rarely does. In the marine environment, to keep everybody content, it would be desirable to have a pristine state at the same time as increasing the productivity of commercial species. Biodiversity effects of fishing are therefore considered troublesome from, at least, two points of view: they jeopardize the production capacity as well as cause a detrimental effect on the natural state of the marine ecosystem. As for production capacity, the question is on which level biodiversity is of importance to protect: species, stock, trophic level or community.

It could be argued that if the target stock is in a bad state, other impacts of concern such as unintentional catches are likely to be so too or not of relevance, and only focusing on stock status. However, this task is not easy and efforts are currently being made by Emanuelsson (in prep), as well as there are exceptions. The economically lucrative lobster fishery in Maine has boomed following depletion of local fish stocks (Steneck et al., 2011); the same situation could to some extent be applied to the Nephrops fishery on the west coast of Sweden. Simply being satisfied with the fact that the crustacean stocks are stable (ICES, 2011) does not necessarily imply that the fishery could be characterized as a sustainable resource use, as it has the potential to affect rebuilding of depleted fish stocks from possible high levels of unintentional catches of depleted fish stocks as well as it could have differences in seafloor area impact, some in no-trawl zones depending on gear use (paper I). Therefore, a range of complementing indicators is needed, in addition to target stock status, in order to assess fisheries sustainability and the environmental impacts.

5.2 Unintentional catches: By-catch and discards

By-catch is the part of the catch that is not directly targeted for. This part could be landed, i.e. brought to market, in general consisting of species with less information regarding stock status. Discard is the part of the by-catch that is directly thrown back to sea for various reasons, such as being of lower economic value, restricted by quota or being under the minimum size for being allowed to be landed. It has been estimated that the weighted average global discard rate in marine fisheries is 8 % (Kelleher, 2005), but this figure varies greatly in time, space and between fishing practices. Some fisheries in the North East Atlantic have the highest discard rates in the world, whereas artisanal fisheries by in general utilizing a greater proportion of the catch, have a lower amounts discarded (Kelleher, 2005; Ziegler et al., 2011). Prior studies have also identified that fishermen involvement and understanding are of great importance to reduce discards (Suuronen & Sardà, 2007; Catchpole et al., 2005b). Discard practices are presently of considerable concern for sustainable resource use, and efficient management to reduce discard is highly ranked on the political agenda in many parts of the world, e.g. in the upcoming reform of the Common Fisheries Policy of the EU.

5.2.1 Non-commercial species in discards

First, it should be noted that different categories of discarded species are subjected to different monitoring effort. Invertebrate taxa are generally insufficiently recorded and are hence excluded from this discussion, even though a study on sensitive non-commercial invertebrate composition in discards in the studied area for the case study (paper 1), showed differences between fishing practices (Ottoson, 2008).

Marine mammals are unintentionally caught in global fisheries, the same occurs in some of the Swedish fisheries (Lunneryd et al., 2004). Globally, some mammals are being at risk of extinction because of high mortality from fisheries, such as the Vaquita porpoise (Avila- Forcada et al., 2012). Unintentional catches of mammals have however brought a lot of public attention, and has created incentives for special eco-labels, such as dolphin safe tuna (Thane et al., 2009).

Birds and turtles are also to a great extent being by-caught in fisheries (Žydelis et al., 2009; Wallace et al., 2010), with efforts made on technical solutions in order to avoid interactions. Marine mammals, turtles and birds would apply as ―charismatic species‖, and would most likely be included in the concept of Endangered, Threatened or Protected (ETP) in MSC assessments, with recommendations to avoid impacts on these case-to-case defined species for the fishery to be certified (MSC, 2011b). Fish and invertebrates in general attract less attention.

5.2.2 Discard of commercial species

Whereas the general importance to decrease discard has to some extent been hard to understand by fishermen (Catchpole et al., 2005ab), discarding fish of landing size (with no survival potential) due to quota restrictions has been more troublesome for fishermen. From a pure resource perspective, discard of juvenile fish is of great concern. It has previously been estimated that an end to discard of cod, haddock and whiting in the North Sea have the potential to increase the stocks with 41%, 14% and 29% respectively in ten years (Catchpole et al., 2007). In stock assessments of many commercial species, juvenile discard is now increasingly included in fishing mortality estimates.

Whereas discards of juvenile fish species is a substantially unwanted impact on fish resources and could impede stock rebuilding (Hutchings, 2000), discards of juvenile invertebrates such as Nephrops is more debated. The high discard ratios of juvenile Nephrops in the trawl fisheries in Sweden (paper I) originates from a high minimum landing size in the region. Castro et al. (2003) suggested that due to the higher survival potential for Nephrops than for many fish species, there is a net positive effect of releasing juvenile Nephrops instead of landing them all, i.e. a discard ban of juvenile Nephrops could prove to be negative for the stock. Having a high discard ratio of commercial invertebrates such as Nephrops, does therefore not necessarily imply that it is of great resource concern, especially if the discards are included in assessments as is the case with Nephrops in the studied area (ICES Advice 2010, Book 6).

For many commercial fish species mainly caught as by-catch, little or no direct management is in place. It has been estimated that approximately 40 % of global landings comes from bycatches, if the definition would include all species lacking sufficient management (Davies et al., 2009). The sensitivity of these fish species to the operating fishing practices in the area would at times only be brought to attention when the decline is obvious and the species could be threatened with extinction (Brander, 1981). Therefore, it is of great importance to increase monitoring and different fisheries‘ effect on these species, especially from the discarded part of the catch, which is rarely visualized.

5.3 Benthic impacts

Different gears have a varying seafloor contact, with demersal trawls, especially beam trawls, having the greatest impact and may cause severe habitat degradation (Watling & Norse, 1998; Hiddink et al., 2006). Seafloor disturbance is not a focus to this thesis, but needs to be mentioned as the area disturbed is quantified in relation to the seafood product in paper I. In

23 the Kattegat area, intensive trawling occurs, affecting the same area often several times per year, leaving parts in a permanently altered condition (Nilsson & Ziegler, 2007). Quantifying the area disturbed should preferably take into account the vulnerability of disturbance caused by different gear constructions as well as the frequency of impact. The information found on the area of impact from a demersal gear is in addition surprisingly scarce.

Even if this area of concern is considered to be outside the scope of this thesis, it should still be noted, that the selective demersal trawls studied in paper I is allowed to trawl in no-trawl zones, possible causing different effect than trawling outside these zones, in addition to having a lower CPUE, i.e. more seafloor area affected per kilo of landing.

6. New approaches for by-catch assessments

6.1 Threatened species

Extinction risks for fish species has for long been thought to be less acute based on observations on a general higher fecundity, abundance and distribution range compared to threatened terrestrial animals (Reynolds et al., 2005). But the perception of an inexhaustible fish resource, reigning up until the great expansion of modernized fishing fleets, has had to be revised. The history of fishing is now known to have left several animal species extinct, or threatened with extinction, and fish stocks have been severely depleted, possibly with little recovery abilities (Jackson, 2001; Roberts, 2007). In e.g. the North Sea, it has been estimated that over 99 % of the biomass of large fish species (16-66 kg) has been removed by fishing (Jennings & Blanchard, 2004).

The primary threats to fish species are over-exploitation and habitat loss (Roberts & Hawkins, 1999; Reynolds et al., 2005). By-catch management has especially been called for, with some long-lived, low fecund and large species complexes such as sharks and rays needing extra mitigation of the impacts imposed by the fishing industry (Hoffman et al., 2010). Related to seafood production, threatened species have so far mainly been considered as an ETP-concept within the MSC labeling scheme, where species listed by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) are in general the most considered (MSC, 2011b). As for fish species on the CITES list, only a few shark species and a handful of bony fish are listed, but with strong law enforcement restricting utilization.

On the other hand, the International Union for Conservation of Nature (IUCN) provides a red list of threatened species on a global, and for some countries, even on a national level (IUCN, 2011). The globally standardized assessment methods are generally based on abundance trends in relation to generation time. The IUCN approach has been shown to be of high consistency both in relation to life history parameters sensitive to fishing pressure (such as older age at maturity, larger maximum size and longer life span) and stock advice from the International Council for Exploration of the Seas (ICES) (Dulvy et al., 2005; paper II). Yet, the national red list of fish species has attracted minor attention to fisheries managers, even if in recent years fisheries has become increasingly restricted or even closed for some of the

24 species listed, such as European eel (Anguilla anguilla) and spurdog (Squalus acanthias), but not all as in the case with e.g. whiting (Merlangius merlangus) (Swedish Board of Fisheries, 2011). The World Wildlife Fund (WWF) in Sweden suggests the consumers to avoid all species occurring on the red list in their seafood guides, unless a stock is certified with an eco- label (e.g. Eastern Baltic cod, KRAV-certified).

The aim with the red list is to provide an alarm signal when a decline of a species is not originating from a regulated exploitation (Mace & Hudson, 1999). This makes the approach ideal for protecting species lacking management, as would be the case for unintentional catches in fisheries. In paper II, it was found that fish species with greater values for age of maturity, life span and maximum length were progressively found in categories of higher threat status, which could make the red list status a carrier for aggregated information on fishing vulnerability. By studying differences in amounts of red listed fish species in discards (VEC; Vulnerable, Endangered or Critically Endangered according the national IUCN red list) between demersal trawling segments in the Kattegat and Skagerrak area, it was found that for every ten kilos of Nephrops landed by conventional trawl, 30 red listed fish were discarded, whereas the equivalent for ten kilos of Northern shrimp (Pandalus borealis) landed with a species-selective trawl, only discarded one red listed fish (paper I). Differentiating sensitivity of impacts from unintentional catches attributed to a seafood product by estimating the mass or individuals of threatened species discarded per landing could serve as an appealing indicator to quantify impacts on sensitive fish species.

Discussions are ongoing on whether protecting dominating species or key stone species, i.e. species with great importance to ecosystem structure, are of greater importance to protect than rare species (Jordán, 2009). However, as the demersal fish biomass in the North Sea is dominated by a few species (e.g. cod, whiting and haddock) (Jennings et al., 2002), finding them all now on a list of threatened species is of great concern from both viewpoints. If formerly dominant species now are rare in relation to historic levels (as is indicated by the VEC approach), the impact potential in terms of ecosystem effects could be seen as alarming, both from a key stone species/dominant/rare species perspective.

6.2 Food web interactions

Species are assigned to different trophic levels (TL) in in the food web, with primary producers having TL=1 and being the most abundant in terms of production, their consumers TL=2, with less mass than for the lower trophic level and so on shaping a pyramidal structure with increasingly less biomass being able to be sustained due to limitations from energetic transfer dynamics. The TL of a species varies e.g. during the species life cycle and season and is therefore not a constant (Jennings et al., 2002), these estimates are coupled with great uncertainties. Estimates of the TL of fish species are at present made from fractional diet composition (found at fishbase.org) or by stable nitrogen isotopes (e.g. Pinnegar et al., 2002). A comparison between the two methods indicated some differences, such as higher trophic levels could be derived by stable nitrogen isotope studies, which are believed to originate from the complexity of predation patterns of soft bottom- and plankton communities.

This thesis‘ focus on trophic distortions is mainly related to how to quantify and differentiate impacts between different fishing practices on trophic energetics, in particular commercial and non-commercial fish and commercial invertebrates in discards. It should be noted that ecosystem dynamics are complex and involve several other species such as marine mammals, reptiles, etc., where fisheries e.g. could cause trophic implications by competing for food or altering competition within the bird complex (Tasker et al., 2000; Cury et al., 2011). However, the attempt made here is to discuss the implications from fisheries with different discard compositions, and how trophic indicators could be interpreted within the LCA framework.

From a pure resource perspective, i.e. effects on the ecosystem‘s potential fish production, it has been suggested that the fish production depend on various factors such as e.g. the number of feeding links (Lindeman, 1942), efficiency of energy transfer (Ryther, 1969; Iverson, 1990), consumer body size (Denney et al., 2002), nutrient availability (Chassot et al., 2007) and species richness (Frank et al., 2007). Top predators have often been exploited at unsustainable levels, causing trophic distortions. As these species in general are slow growing with low reproduction rate, this has led to the depletion of many predatory fish stocks (Christensen et al., 2003; Myers & Worm, 2003), which make this impact a concern even from a threatened species perspective (paper II). The trophic implications of the depletion of top predators in terms of ecosystem functioning are not clear, but uneven targeting patterns on top predators have been shown to cause regime shifts (Casini et al., 2009). Different geographical regions have however been found to have varied energy dynamics, with evidence for top down (predator) control as well as established bottom-up (primary producer) controlled trophic linkages (Frank et al., 2005; Ware et al., 2005). Energy transfer control can also be dependent on a few species at intermediate trophic level controlling the energy transfer between upper and lower levels, called ―wasp-waist‖-ecosystems (Cury et al., 2000). It has been suggested that due to the sequential depletion of top predators, fisheries are forced to increasingly turn to species at lower trophic levels, known as ―fishing down the food web‖ after it was shown in global landing statistics as a decreased mean trophic level of landings (MTL; Pauly et al., 1998).

Mean trophic level (MTL) of fisheries landings is at present an operational indicator for the Convention of Biological Diversity (CBD) as ―Mean trophic index‖ (MTI) and is stated as an indicator ‗ready for global use‘ (CBD, 2010). The findings by Pauly et al. (1998) have since then however been heavily debated in terms of what could possibly be interpreted from using landing data, which is affected by changes in management such as quotas and gear usage (Branch et al., 2010), and somewhat revised, with new concepts such as e.g. ―fishing trough marine food webs‖ (Essington et al., 2006) and a ―fishing in balance‖-index (Pauly et al., 2000). In Hornborg et al. (paper III), the management effect on MTL is further reinforced by studying MTL in official landing statistics, survey data and total catch (including the discarded part) in separate demersal trawling segments in the same area (Kattegat and Skagerrak). The results showed that it is evident that e.g. turning to species selective trawling for invertebrates would result in a lowered MTL of landings, which is unwanted from the CBD perspective. The same effect on MTL would arise from conventional trawling for e.g.

Nephrops when quota restrictions on depleted fish stocks are enforced. The great difference in terms of possible ecosystem effect would be in the MTL of the total catch (or the discarded part), further reinforcing the necessity to use catch data instead of landing data when evaluating the MTL indicator trend globally (sensu Branch et al., 2010).

Closely related to MTL is the concept of Primary Production Required (PPR) from fisheries landings. PPR is an estimate of the amount of carbon that has been needed to produce one kilo of wet weight of a species at a certain trophic level (Pauly & Christensen, 1995). PPR is estimated from assuming a 9:1 ratio for conversion of wet weight to carbon (Strathmann, 1967) and using estimates of transfer efficiency (TE), i.e. the proportion of production that is retained in transfers between each trophic level (TL) (Lindeman, 1942). TE varies between e.g. ecosystems, but has been suggested to have a global mean of 10% (Pauly & Christensen, 1995). The PPR estimate thus assumes that fish production is limited by carbon transfer, that it is a constant transfer along the food chain and independent of the length of the food chain. It must be acknowledged that all of these assumptions could be discussed (Baumann, 1995). Due to the great uncertainties surrounding estimates of TE and TL, comparative studies on PPR from fisheries from different regions using either differentiated TE or the global average of 10 % is dubious. Short transfer chains (e.g. in upwelling areas) have relatively robust PPR estimates, as fewer links are involved (and hence the sensitivity to differences in TE values), as well as the fish species occurring in general have a lower trophic level (which have lower TL uncertainty). On the other hand, longer transfer chains (e.g. temperate shelves areas), are much more sensitive to even the smallest uncertainty in trophic level or trophic efficiency, resulting in greater uncertainties to the PPR estimate (Baumann, 1995).

The PPR concept implies that exploiting species with different TL differs in terms of ecosystem cost (Pauly & Christensen, 1995), where the currency is PPR, and a higher value per landing is a greater disturbance to the ecosystem than a lower (ICES, 2005). It must be noted that there are regional differences between possible impacts (Frank et al., 2007), where e.g. the highly nutrient rich Baltic Sea would be at one side of the scale, and the oceanic systems on the other (Conti & Scardi, 2010). In addition to this, exploiting fish species at lower trophic levels (with a lower PPR) could also only be considered to be sustainable up to a certain limit in terms of absolute quantities, without causing effects on the upper trophic levels (Smith et al., 2011).

The percent of available primary production required from fisheries varies between regions, with the heavily exploited continental shelves having a value between 25-35% (Pauly & Christensen, 1995). This level of appropriation is high, as it has been suggested that only 41% of the coastal phytoplankton is at all consumed and moved up through the food web (Duarte & Cebrian, 1996). Upwelling areas show the highest %PPR from fisheries, with lower probabilities of sustainable exploitation at current exploitation rate (Coll et al., 2008; Chassot et al., 2010). The highest and long term sustainable fishing yields have been shown to occur from a combination of moderate fishing pressure and catches having a low to moderate MTL (Conti & Scardi, 2010).

Evaluating Swedish fisheries landings on the west coast during the last century with the trophic indicators MTL and PPR identified constraints to present use, as well as what could possibly be interpreted from the indicators (paper III). According to these findings, MTL is better used to evaluate the relative trophic impact from a fishing gear or targeting behavior within the same region. Demersal trawling could have between 5 -80 % of the PPR from the landed part depending on gear and targeting behavior. If the fishery is mainly performed by selective trawling for invertebrates or by mixed trawling, MTL and PPR per landing will be affected differently. Selective trawling for invertebrates would decrease PPR per landing, in line with the requirements for a more sustainable resource use (Coll et al., 2008; Chassot et al., 2010; Swartz et al., 2010); on the other hand, MTL of landings would simultaneously decrease, which is an undesired outcome to the CBD.

Increased routine assessments of PPR of discard are valuable for better estimates of the true level of resource use. Coll et al. (2008), in lack of true values, added different theoretic levels of PPR from discard when evaluating the long term sustainable yield of fisheries per Large Marine Ecosystem (LME). The probability of being sustainably fished was increasingly lowered with higher discard PPR assumed, indicating the importance of including this part of resource use as well. In line with this, it has also been suggested that PPR standardization enables marine footprints to be compared between different fisheries (Swartz et al., 2010). For this to be operational, it is necessary to use catch data instead of landing data. In environmental systems analysis of seafood production, discard PPR could be compared with feed appropriation of primary production in aquaculture, assessed before as Biotic Resource Use (Papatryphon et al., 2004). The PPR approach for discards clearly show that discards are a hidden cost of fisheries: discard PPR from capture fisheries can be in the same range as the appropriation of feed production used in salmon culture per kilo of live weight salmon (paper I; Pelletier et al., 2009). It is however important to combine the PPR value with information on sensitive species affected, such as the VEC-approach (paper II). Little can otherwise be said when comparing different values of PPR from discards (as is done in Vázquez-Rowe et al., 2012).

For PPR to be considered as an impact of resource limitation, the value must be placed in a historic context (paper III). Even if it has been suggested that European seas are controlled by bottom-up processes (Chassot et al., 2007), it must be noted that the primary production in the studied area (Kattegat-Skagerrak) increased due to eutrophication from levels around 100 g C/m2 in the 1950s to 200 g C/m2 in the 1990s (Richardson & Heilmann, 1995). This increase has even been suggested to cause increased yields in pelagic fisheries in the Kattegat in the 1950s-1970s (Nielsen & Richardsson, 1996). However, with time, total landings have decreased in the area. The ecosystem at present leave primary production ―underutilized‖, with detrimental effects on coastal habitats such as hypoxia (Pihl, 1994), possibly a combination of eutrophication and fisheries ecosystem effect on functional biodiversity from uneven targeting patterns.

Last but not least, it should be noted that using theoretic TL, MTL and PPR values, little can be said on true ecosystem implications of Swedish fisheries during the last century. Herring is, and has been, dominating in terms of quantity in Swedish landings (paper III). This is one

28 of the few species that has been found to not have a strong positive relationship between increasing size and trophic level- as well as it has shown to have a decrease size spectrum as fisheries exploitation progress (Jennings et al., 2002). This implies that the bulk of Swedish fisheries landings (i.e. herring) could in fact have increased in trophic level with fishing exploitation. In the Baltic, another amplifying effect of TL change is the introduction of the invasive fish-hook water flea (Cercopagis pengoi), where changes in the zooplankton community increased the trophic level of herring in the Baltic from 2.6 to 3.4 (Gorokhova et al., 2005). Both these facts illustrate important divergence between trophic level estimates and the not accounted variability found in the ecosystem, with great implications to historical patterns of MTL and PPR in fisheries.

To conclude, by promoting different gears and setting quotas for species based on the total catch PPR value instead of merely landings, a step towards Ecosystem Based Fisheries Management (EBFM) is made. However, as the PPR does not say anything of the status of the species in the ecosystem (i.e. if species discarded are overexploited or of no concern), makes it important to complement PPR with information on the sensitivity (such as VEC; paper II).

7. Fisheries management and LCA

The major contribution so far from environmental systems analysis of seafood production is the coupling of abiotic resource use and impacts, such as fossil fuel need and greenhouse gas emissions to a seafood product. It has been estimated before that a global average of 0.62 liters of fossil fuel is burnt per kilo landings (Tyedmers et al., 2005). However, as global landings are dominated in mass by pelagic fisheries (FAO, 2010), highly energy efficient per kilo of landing (Thrane, 2006, Tyedmers et al., 2005), other fishing methods, such as demersal trawls, have been found to have considerably higher fuel requirements per kilo of landings (Ziegler & Valentinsson, 2008). Energy use per kilo of flatfish can e.g. be 15 times higher using a beam trawl compared to Danish seine (Thrane, 2006). Due to differences in energy consumption between capture methods, in combination with the findings that the fishing phase is the most important contributor to the energy needed during the life cycle of a seafood product (Ziegler et al., 2003; Thrane, 2006; Ziegler & Valentinsson, 2008; Magerholm Fet et al., 2010), management of the fishery is of great importance for the outcome of the environmental impact from a seafood product from capture fisheries (Winther et al. 2012). Decisions on e.g. gear use (Vázquez-Rowe et al., 2010; paper I) have a potential to strongly affect the total outcome of seafood LCA‘s.

The broadened perspective that a LCA evaluation brings is also of cumulative importance to fisheries management, from both an environmental as well as an economic perspective as the fleet is highly depending on fossil fuel that is becoming increasingly scarce and expensive. Several environmental impacts attributed to a seafood product can be seen as a failure of management. Overexploitation (decisions on quotas, fleet size, effort and lack of observance) leads to a lower landing per unit effort (LPUE). Lower LPUE results in longer fishing time to land the same amount, with increased total fuel consumption, possible greater seafloor disturbance and increased discards when compared within the same fishery. As fuel use in fisheries has not so far been a concern to fisheries management, but instead has been

29 encouraged by vast subsidies, this neglect is resulting in a net income loss from fishing to society (Arnason et al., 2008) as well as an increasing energy need per kilo of seafood product (Tyedmers, 2004; Schau et al., 2009), preventing necessary structural adjustment in the fleet.

Two previous LCA studies have quantified the direct implications of fisheries management decisions on energy use and accompanied GHG emissions. The first was a case study on the New England Atlantic herring fishery (Driscoll & Tyedmers, 2010). By looking at the effect of altered management regulations on gear and quota allowances, the study identified a range between 21-116 liters of diesel per ton of landed herring; with a totaling range between 945 000-5 220 000 liters to fill the quota. Discard differences between gears were stated in the study, but there was no further elaboration on the biological implications in relation to the fuel need. In the second study, biological impacts (such as differentiated discard impact and seafloor area affected) was quantified in parallel with energy need of the Nephrops caught in the demersal trawl fishery on the Swedish west coast (paper I). In this study, a trade-off between local (the protection of local stocks) and global effects (increased GHG emissions and fuel use) of management decisions regarding the promotion of a species selective trawl to protect local cod stocks was visualized.

The result from the two case studies clearly shows that even if rebuilding of stocks is possible and underway (Worm et al., 2009), it is important to quantify seafloor impact, fuel use and discards coupled to harvest of the decided TAC, effort and gear regulations. Fuel use and other biological impacts from fisheries do not necessarily go hand in hand, and even act in opposite directions during stock rebuilding if selective demersal trawling is promoted in order to protect collapsed fish stocks (paper I). Acknowledging potential trade-offs outside present management consideration is a necessity when aiming for an ecosystem based management and an overall improved resource use.

This concern is of increasing importance with respect to present movement towards selective gears in order to e.g. minimize interactions between fisheries targeting stocks in good condition and rebuilding depleted stocks (Hall, 1996; Catchpole et al., 2005b). Within the European Union, a discard ban currently under discussion within the reform of the EU Common Fisheries Policy (CEC, 2009) is boosting the process by suggesting more selective practices. Some passive gears, such as creels, targeting the same species, have been shown to have lower fuel intensity relative to active gears as well as with less seafloor impact and lower discard rate with higher survival upon release (Ziegler & Valentinsson, 2008). Promoting selective demersal trawls, that are likewise energy intensive and destructive in terms of seafloor disturbance as other demersal trawls (but have a lower catch per unit effort), are however more challenging in a broader context to be used to protect stocks (paper I). Which environmental trade-offs are acceptable for protecting depleted local fish stocks? From an LCA perspective, it would be superior to promote the best available technology (in this case creeling) and to cut the trawling fleet, instead of making it less effective. This could also prove to be favorable from a socioeconomic perspective, as increased fuel costs in combination with decreased landings from overcapacity have been and are troublesome to the general profitability of the Swedish fishery (Bengtsberg, 2007).

When studying the fuel intensity in the whole Swedish demersal trawl and seine fishery in the last decade, a trend of decreasing fuel use is however now seen (Andersen & Guillén, 2010). The landing per unit effort has in general increased, but with a constant fuel use per effort, the decreased effort result in increased fuel efficiency (Ziegler & Hornborg, in prep.) It would have been interesting to know what an even stronger capacity cut would have done for the total fuel consumption in Sweden in relation to the movement towards energy intensive gears with lower LPUE such as selective trawls. Of the total mass of landings by demersal trawls and seines in Sweden, Nephrops only represents around 5 %, which means that the overall result of the species-selective trawling having higher fuel consumption per kilo of landing is undetectable in statistics when aggregated in national fleet segments (demersal trawling is dominated by Baltic cod trawling). With this argument, the increase of fuel need per kilo of Nephrops by selective trawling could be considered a small problem, given its minor contribution to the total fuel consumption of the fleet.

Finally, a small economic note should be made. As there has been a minor increase in proportion of Nephrops in demersal landings in mass in comparison to the relative value of the species in the catch (figure 2), and as at the value of Nephrops have been relatively stable during the time period (at approximately 9-10 Euro/kg), the decreased fish landings in the trawl fishery has increased the economic dependence on Nephrops. Due to the relatively high price of Nephrops landings, turning to selective trawling for Nephrops in Sweden has been successfully implemented, even if it can be considered to be forced from effort restrictions on trawling catching cod (paper I).

Figure 2. Percentage of total value and mass respectively attributed to the Nephrops part in demersal trawls in Sweden (Andersen & Guillén 2010).

A study on the profitability of selective trawling for Nephrops showed that in terms of short- term profitability, selective trawling could be troublesome but more profitable in the long term (Macher et al., 2008). However, it should be noted that the development of a fishery towards highly priced single species due to depletion of other stocks is sensitive, both from an ecological and socio-economic perspective (Steneck et al., 2010). It might be proposed that instead of turning to selective trawling practices (due to depletion of fish stocks), new approaches, such as other gears deployed and greater areas protected from fishing to rebuild fish stocks, should be enforced until overcapacity is resolved. Most recently, general concerns

31 have also been expressed on the ecosystem effects of selective fishing, propagating for utilizing a mixed size and species catch (Garcia et al., 2012).

9. Conclusions and future outlook

This thesis combines the abiotic assessment framework of LCA with the biotic impacts of fisheries and fisheries management and contributes to increased assessment of unintentional catches within the LCA framework.

It was found that two complementing discard indicators are needed. PPR in discards does not reveal anything on impact of sensitive species (VEC), which therefore is an important complement. As for applying VEC globally in seafood LCA‘s, IUCN assessments must increase their coverage of marine fish species. The PPR approach must also be made with caution, as the values must be placed in the right context (such as nutrient availability) and which transfer efficiencies values that should be used when comparing seafood products from different regions. By adding information on discard quantity of threatened fish species (VEC) in combination with the primary production required (PPR) to produce the discard, environmental assessments of seafood production can move towards a more integrated approach, at least in terms of impacts from unintentional catches.

By using a life cycle approach, broader evaluations of fisheries management can be made, visualizing not considered potential trade-offs in an integrated format. This is of increasing importance to fisheries managers to achieve an overall sustainable resource use in world fisheries. It is time to shift gear and turn to the best practice in the longer and broader perspective. Instead of quick fixes, such as promoting selective demersal trawls to mitigate wasteful discards, changes to reigning policies in line with the discussions in Garcia et al. (2012), or promote other types of gear that are not questionable in a broader perspective, must be made.

Planned future work will be focused on size selectivity. The selectivity of the gear is not only the main reason behind different quantities of unintentional catches, but also different size exploitation of the targeted species. As fishing normally target larger individuals in an exploited stock, due to high value and restriction on minimum landing size, there is an increasing concern for ―fisheries induced evolution‖. This concept implies that the targeting of the largest individuals put evolutionary selection pressure on certain individuals, resulting in progressively smaller individuals/mean size and lower yields of the exploited species (Conover & Munch, 2002; Kuparinen & Merilä, 2007). A size related indicator of fishing impact is therefore of high relevance (Jennings et al., 2002), and could in theory combine the VEC and PPR approaches for both target and by-caught fish stocks. Species of high trophic level most often have a high Lmax and are more often found on the IUCN‘s red list of threatened species. Larger species are also most often top predators. By shifting focus to cod stock management in the coastal areas of Sweden, including the Baltic Sea, this issue is to be further explored.

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Paper I: Integrated environmental assessment of fisheries management: Swedish Nephrops trawl fisheries evaluated using a Life Cycle approach

Sara Hornborgab*, Per Nilssonb, Daniel Valentinssonc & Friederike Zieglera. a Swedish Institute for Food and Biotechnology, Sustainable Food Production, Sweden b University of Gothenburg, Department of Marine Ecology, Sweden c Swedish University of Agricultural Sciences, Department of Aquatic Resources, Institute of Marine Research, Sweden

*Corresponding author: tel. +46-10-5166696 fax +46-31-833782 email: [email protected]

Abstract Fisheries management needs to broaden the perspective to achieve sustainable resource use. Life Cycle Assessment (LCA) is an ISO standardized method to evaluate the environmental impacts of a product using a broad and systematic approach. In this study, the outcome of a management regime promoting species-selective trawling in Swedish Nephrops trawl fisheries was studied using LCA methodology by quantifying the impacts per kilogram of landing using two different methods. Demersal trawling has previously been found to be both energy intensive and destructive in terms of seafloor impact and discards. It is demonstrated that species-selective trawling fulfills management objectives, although with tradeoffs in terms of fuel consumption and associated GHG emissions. To prioritize between impacts, one must be aware of and quantify these potential tradeoffs. LCA could be an important tool for defining sustainable seafood production as it can visualize a broad range of impacts and facilitate integrated, transparent decision making in the seafood industry. It is also concluded that, with current LCA methodology, use of total discarded mass could increasingly be distinguished from potential impact by applying two new concepts: primary production requirements and threatened species affected.

Keywords: LCA, Fisheries management, Nephrops, Discard, Fuel

1. Introduction Managing fisheries is complex. Measures are often determined based on uncertain data, in a limited time, and with a range of different motives – economic, social, and biological – predominantly lacking the integrated perspective [1]. Several current fishing regimes have been found to have severe negative impacts, not only on targeted species, but also on whole marine ecosystems, and are accordingly being questioned [2,3]. Discussions of sustainable fisheries management have focused mainly on stock recovery and sustainable exploitation rates [4], whereas possible consequences of measures taken to improve or sustain stock status, such as increased energy consumption or seafloor disturbance, are seldom integrated in the same management context. This may result in incoherent management decisions, which in turn lead to overcapacity and fuel subsidies.

Besides improving fisheries economics [5], there is a cumulative need to mitigate the net effects of a range of anthropogenic stressors on the marine environment [6]. The need for an overall evaluation of the impacts of management measures can be seen in recent developments such as increasing consumer awareness and the ongoing reform of the EU Common Fisheries Policy [7,8]. Broader approaches, such as strategic environmental assessments (SEA), are asked for to pre-evaluate expected impacts of proposed fisheries management measures in the EU [9]. As a complement, there is a need for the post-evaluation of broader environmental impacts of measures taken, in order to increase the transparency of the seafood sector.

1.1. Life cycle assessment and seafood production

Life cycle assessment (LCA) is an ISO standardized methodology that relates resource use and environmental impacts to a product from a cradle-to-grave perspective [10]. In seafood production, early LCAs generally concluded that, of traditional impact categories, such as greenhouse gas (GHG) emissions, the fishing phase dominated the life cycle due to the fuel intensity [11,12]. Fisheries management, by influencing, for example, the type of gear used, may have implications for the resource use of fisheries. Overcapacity and decreasing fish stocks are expected to lead to excess effort, which could in turn influence fuel consumption [11,13–15]. By shifting from a product to a management perspective, LCA could provide a comprehensive and transparent evaluation of the overall environmental implications of fisheries management measures by comparing the environmental impacts per seafood product, revealing the magnitudes of impacts and the potential trade-offs between them. So far, the only study using LCA to evaluate various fisheries management scenarios identified a range of 17-116 l of diesel per ton of landed herring [16]. However, biological impacts were not to a great extent taken into consideration as is attempted here. If one considers biodiversity loss [17], fish stock depletion [7], trophic interactions [18], size alteration [19], and seafloor disturbance [20], which are not usually considered at present [21], the impacts of fishing become even more serious. The problem has been lack of methodology. One study that tried to gauge discards and seafloor area disturbed per kg of landed Norway lobster (Nephrops norvegicus) indicated vastly different biological impacts for different fishing practices: 15,000 m2 of seafloor was found to be affected by trawling while creeling affected only 1.8 m2 of seafloor, with total discards of 4.5 kg versus 0.36 kg [22]. The present study considers differences in appropriation of primary production from discards as a differentiated discard impact in an LCA framework. Primary production requirements (PPR) are considered, because primary production limits global fisheries yield [23] and gives a rough proxy for trophic interactions such as depletion of top predators, an established fisheries impact [17,18]. A new LCA category included is the potential discard impacts on vulnerable, endangered, and critically endangered (VEC) fish species [24]. Fisheries are often the reason why fish are under threat, so it is important that this impact should inform practice. The International

Union for Conservation of Nature (IUCN) Red List is intended to protect species not specifically covered by a management framework, as is often the case with discarded species, and has been shown to be adequately correlated with the results from stock assessments [25,26]. Landed fish species are not included, but are considered as a managed, hence controlled, impact.

1.2. Case study: the Swedish Nephrops fishery

Norway lobster (Nephrops norvegicus) is one of the most valuable species in Swedish fisheries. The fishery is located in the western coastal waters, the Skagerrak and Kattegat (ICES area IIIa SD 20 and 21, Fig. 1) and is conducted using demersal trawls and creels. The recommended and agreed-on total allowable catch (TAC) for the area was 5170 tons in 2010, of which the Swedish portion was 1359 tons [27].

Fig. 1. ICES area IIIa SD 20 and 21.

The Nephrops trawl fishery in the North-east Atlantic is known to have one of the highest discard ratios in the world [28]. Discard is the portion of the catch that is thrown back to sea, in amounts that vary strongly with, for example, area fished, season, management policies, economic incentives, and fisherman behavior. In Nephrops trawl fisheries, by-catch consists to a great extent of fish species many of which are restricted with quota. To decouple Nephrops catches from quota-filled fish species and keep the fishery open when quotas on other species are closed, in 2004, the Swedish Board of Fisheries developed and implemented a species-selective grid of Nordmᴓre type (Fig. 2) which releases fish through an escape window [29].

Fig 2. The Nephrops sorting grid (illustration: Jürgen Asp). Fishing days permitted with conventional trawls have gradually been reduced since 2004 in accordance with long-term management for cod recovery by reducing fishing mortality of cod [30, 31]. Vessels trawling without sorting grids are restricted by both TAC and effort measures in line with the updated Cod Recovery Plan [31]. Grid trawling is excluded from effort regulation due to low by-catches of cod, only being subject to a national level effort limitation [32]. Furthermore, vessels with sorting grids are allowed access to some areas closed to conventional trawling, such as a no-trawl coastal zone and parts of a marine protected area in the Kattegat (Fig. 1). From having been mainly a mixed fishery, catching Nephrops and fish, grid introduction has led to the development of a separate single-species fishery for Nephrops [33]. In 2009, grid trawling accounted for 50% of total Swedish Nephrops landings; conventional trawling landed 30%, while creeling landed the remaining part (Fig. 3). Selective fishing practices, however, may not reduce overall pressure on the marine environment, as landings per effort are lowered for gear that in this case are already characterized by high fuel consumption [11,14,22] and seafloor disturbance [20]. Species- selective fishing is more vulnerable when catches of Nephrops are low, and could accordingly increase resource wastage. At the same time, use of sorting grids could represent an improvement, as sorting time decreases, contributing to higher quality and mitigating overcapacity. Expert opinions on marine ecosystem stressors urge immediate action to reduce GHG emissions and restore the structure and function of marine ecosystems [34]. It is therefore important that broader evaluations establish a proper framework for determining whether cutting the fleet or making it less effective would contribute most to reaching management goals.

Fig. 3. Contributions of different types of gear to Swedish Nephrops landings, 1999–2010.

1.3. Aim of the study

The present study aims to evaluate the broad environmental implications of having the Nephrops trawl fishery in Sweden structured into two separate fisheries in response to EU regulations to protect cod. This will be done using LCA expanded with biological impacts. More specifically, potential tradeoffs between the environmental impacts of introducing the species-selective grid, such as increased seafloor area swept or fuel consumption, are quantified in relation to possible biological implications, such as discard impact on threatened species (VEC) and trophic interactions (PPR). An additional aim is to advance the development of LCA methodology with regard to the inclusion of indicators of differentiated discard impact (VEC and PPR) in the framework. 2. Methods

2.1. General life cycle assessment (LCA) methodology

LCA consists of four phases: goal and scope, inventory, impact assessment, and interpretation of results. During the goal and scope phase, system boundaries for the study are defined and the product of focus, i.e., the functional unit (FU), is specified. In the next step, inventory, all resource use and emissions of interest according to the goal and scope are quantified in relation to the functional unit. In the impact assessment, collected data are grouped in categories of potential environmental impact. The most commonly used impact category is global warming potential (GWP), in which all GHG emissions caused in the product‘s life cycle are grouped and weighed together according to the latest scientific findings of the Intergovernmental Panel on Climate Change (IPCC). During the interpretation of results, the robustness of the results is tested, for example, by sensitivity- or uncertainty analysis. The main areas of application of LCA results are in product development, environmental management, and communication (e.g., eco-labels).

2.2. Methodological choices for this study

LCA was chosen because it is the most holistic product-oriented method for assessing environmental impacts and can identify improvement potentials [16,35–37], and because of a general interest in using LCA as a management tool. This particular fishery was chosen to build on the findings of an earlier study [22] of the wider environmental implications of promoting sorting grid use in trawl fisheries. System boundaries include Swedish trawl fishing operations targeting Nephrops in terms of fuel production and consumption, seafloor disturbance, and impacts of discards and landings (Table 1). The time frame is one year, 2009, providing a snapshot of the fishery. Production of fishing vessels and gear was not included because they are known to make a minor contribution to the total result [38], especially in resource-intensive fisheries such as trawling, and are also an equal background system, since the same boats use both types of gear. The functional unit (FU), 1 kg of landed total catch, was chosen because this is the managed output of the different fishing fleets and because grid landings are replaceable with landings from conventional trawlers targeting Nephrops, regardless of species composition.

Table 1. Resource use (fuel) and impacts assessed per functional unit in this study.

Impact Unit

GWP CO2e

Fuel use liters diesel

Total discard kg

PPR kg C

VEC individuals of threatened species (Vulnerable, Endangered or Critically endangered according to IUCN criteria)

Target stock qualitative + kg juveniles discarded

Seafloor m2

2.3. Data sources, assumptions, and limitations

All studied impacts were analyzed separately for Kattegat and Skagerrak, as some differences between the areas, such as marine habitat, species distribution, and, to some extent, different management measures, could affect results. A marine protected area in the Kattegat affects the fishing grounds available for the gear and the no-trawl coastal zone extends three nautical miles in the Kattegat, versus four nautical miles in the Skagerrak. The sampled trips belong to Nephrops-targeted operations as defined by the Board of Fisheries, i.e., a minimum of 10% of the landings by mass consist of Nephrops. Discard survival rate was set to zero, although gear type and species exhibit differences, as too many factors interfere in order to include survival rates [39]. A fuel consumption model based on installed engine power (kW) [40] was applied to Swedish logbook data and adjusted to usage of only 40% of kW during trawling, based on estimates from interviews with fishermen (12 boats landing approximately 25% of the Nephrops trawl landings). A vessel‘s diesel consumption per trawling hour is assumed to be approximately

46 the same whether or not the grid is used, although absolute figures could be influenced by differences in trawling depth, gear configuration, speed, location, and weather [41]. Energy use per landing is hence mainly affected by catchability. A maximum transportation speed was applied to every first haul in a day, assuming 2 h for grid trawling in the Skagerrak (3 h for conventional) and 1.5 h for grid trawling in the Kattegat (2.5 h for conventional). Model assumptions are tested in a sensitivity analysis. Data collected and compiled by the Board of Fisheries on absolute annual fuel use by fishermen were not made available in a format detailed enough for the purpose of the present study for confidentiality reasons, but were used for double-checking. Combustion figures for diesel (MK1) were taken from the Swedish Petroleum & Biofuel Institute (www.spbi.se). In terms of seafloor disturbance, area swept was assessed by differentiating between the proportional use of single versus double trawls. Gear indices were based on data from Nilsson and Ziegler [42], i.e., 0.22 km2 h–1 for single trawls versus 0.39 km2 h–1 for double trawls at an average trawling speed of 2.5 knots, and applied to logbook data.

2.4. Data analysis and impact assessment

Based on earlier LCA results for capture fisheries in combination with our own beliefs as to what approximately characterizes a sustainable fishery, we limited the environmental impacts studied to fuel use with associated GHG emissions, discards (i.e., total discard quantity), PPR, VEC, seafloor area swept, and a qualitative discussion of target species impact (Table 1). Inventory data included were discard quantity, target juveniles caught (see Ziegler et al. [43]), and seafloor area swept [see 22,42,44]. As for impact assessment, GWP [45] and Biotic Resource Use (BRU) [46] have previously been included in the LCA context. BRU captures the amount of carbon from primary production needed in aquaculture to produce 1 kg of wet weight of the cultured species. In this study and for capture fisheries in general, this is better addressed for what it is, i.e., PPR, as was the original intention of the equation [47], because PPR is only one component of the slightly vaguer BRU concept. Species discarded that have a regional status in Sweden as critically endangered (CR), vulnerable (VU), and endangered (EN) in compliance with IUCN criteria [24], together with (in this case) species under regional protection (Swedish Board of Fisheries, www.fiskeriverket.se), are included as individuals of VEC species discarded per functional unit.

3. Results

Some of the inventory data are only presented as inventory results, while others are characterized.

3.1 Target stock

The definition of the fleet resulted in coverage of 96% of trawl landings. Sorting grid- equipped trawls effectively sorted out undesired fish species according to both logbook and observer data (Fig. 4a,b). Fig. 4b describes the species composition of the functional unit.

Fig. 4a. Catch composition by mass from observer data. Top row, Kattegat conventional (left) and grid trawl (right); bottom row, Skagerrak conventional trawl (left) and grid trawl (right).

Fig. 4b. Landing composition by mass as reported in logbooks. Top row, Kattegat conventional (left) and grid trawl (right); bottom row, Skagerrak conventional (left) and grid trawl (right).

The main fish species protected by grid use are cod (Gadus morhua), haddock (Melanogrammus aeglefinus), hake (Merluccius merluccius), and saithe (Pollachius virens). For conventional trawlers, cod accounted for 20% of the landings (25% of catch) by mass in the Skagerrak and 8% (9% of catch) in the Kattegat (Fig. 4a,b). Grid trawling caught mainly flatfishes and juvenile Nephrops, notably Common dab (Limanda limanda) in the Kattegat.

As for impact on Nephrops stock, Sweden landed a total of 1331 tons of Nephrops in 2009 (quota 1359 tons). In mass, Nephrops accounts for 96–97% of the landings in grid trawling; in conventional trawling, Nephrops accounts for 63% of the landings in the Kattegat and 40% in the Skagerrak. The economic value of the Nephrops part of the landings was 98% for grid landings in the Kattegat (87% for conventional); in the Skagerrak, the economic value of the Nephrops part was 99% for grid landings but only 75% for conventional trawl landings. The Nephrops stock in the Skagerrak and Kattegat is currently considered as being exploited sustainably at a level below a proxy for MSY [48].

Conventional trawling in the Skagerrak was also found to produce a low amount of discarded juvenile Nephrops compared with the other categories studied (Table 2). A high amount of discarded Nephrops does not necessarily have to represent a significant target stock impact. Discards have been included in assessments since 1999 and the high discard rate is coupled with a large minimum landing size (40 mm carapace length), which allows reproduction before being landed [49]. The total effect on the Nephrops population is unknown, but it has been suggested that release of juvenile Nephrops reduces instant fishing mortality [50]. According to fishermen, the grid sorts out the largest individuals limited by the distance between the bars, possibly reducing stock impacts as larger females are more fecund.

3.2 Discard quantity and composition

Discard quantity and species composition differed considerably between the two kinds of trawling (Table 2). Grid trawling in the Kattegat produced the highest amount of discard/FU. However, the main portion of discard species in conventional trawling consisted of valuable and quota-restricted fish species such as cod, haddock, and whiting (Merlangius merlangus); in grid trawling, mainly juvenile Nephrops were discarded, in the Kattegat together with flatfish of low economic value, such as small dab.

Table 2. Discard data per FU (with s.e.); hauls were aggregated into boat means.

Gear and area No. No.sampled No.hauls Total Nephrops VEC PPR vessels trips discard (kg) discard (kg) (No.) (kg C)

Skagerrak grid 8 11 21 1,3±0,1 0,70±0,1 0,5±0,1 31±6

Skagerrak 8 12 22 1,2±0,4 0,17±0,1 3,2±0,1 120±37 conventional Kattegat grid 5 12 23 2,5±0,5 0,81±0,2 1,0±0,4 88±22

Kattegat 7 14 27 1,7±0,3 0,75±0,2 2,7±0,6 89±19 conventional

The high dab occurrence in Kattegat grid trawling could be because conventional and grid trawling are more spatially separated in the area (Fig. 5). Survey data have indicated that the occurrence of juvenile dab is much higher closer to the coast.

3.3 Seafloor and energy use

Trawling intensity is heavily aggregated (Fig. 5), making certain areas more affected than others. The highest intensity of seafloor disturbance is found within four nautical miles of the coast in the Skagerrak, an area open only for grid trawls and passive fishing gear.

Fig. 5. Aggregated trawl effort for conventional (left) and grid trawling (right) in 2009. For the Skagerrak, single trawls dominate grid trawling practice, representing 74% of effort, whereas single trawls account for only 47% of conventional trawling effort. In the Kattegat area, generally higher use of double trawls (almost 70% of the trawl effort of both practices) resulted in a slightly higher seafloor disturbance per kilogram of Nephrops for both types of gear than did grid trawling in the Skagerrak. Based on these differences, the seafloor area swept per kg of Nephrops was in the range of 10,000–22,000 m2, with conventional trawling in the Skagerrak contributing to the lowest value and grid in the Kattegat twice the value. Fuel consumption varied between 1.3–2.4 l of fuel consumed per kilogram of landings, with Skagerrak conventional trawling being the most energy-efficient practice and grid trawling needing nearly twice the amount per landing. These results were tested in a sensitivity analysis.

3.2 Overall resource use and impact assessment results

All inventory data and impact assessment results are presented in Fig. 6; inventory data, such as seafloor area swept and discards, are included in the same graph as these results are relevant without defining the potential impact. Conventional trawling generally used less fuel and disturbed less seafloor area per kilogram of landings than did grid trawling; however, grid trawling is superior in protecting threatened species.

Fig. 6. Relative contribution (value of 1 is average of all practices) to mean levels of trawling impact for 1 kg of landings of the four fishing practices.

3.3. Sensitivity and uncertainty analysis

3.3.1. Change of functional unit

If the aim is to keep the trawl fishery for Nephrops open, evaluating impacts per kilogram of landed Nephrops could be of interest. Choice of adequate general allocation method has been debated before [51,52], but, justified by the fact that conventional trawling targets the most profitable mix and grid trawling was developed to catch the economically important Nephrops, impacts are allocated between Nephrops and fish landings based on the percentage of total economic value (Fig. 7). Note that the remaining allocated figures for landed fish species should not be used separately.

Fig. 7. Economic allocation in mixed fisheries; example taken from diesel use in conventional trawl fishery for Nephrops in Kattegat. The dominant trawl practice in terms of contribution to Nephrops landings is single grid trawl in the Skagerrak area (28% of trawl landings). The new results indicated little if no tradeoffs per kilogram of Nephrops caught with grid, only fewer threatened fish caught and a lower PPR (Fig. 8).

Fig. 8. Relative contribution (value of 1 is average of all practices) to mean levels of trawling impact for 1 kg of Nephrops after economic allocation.

3.3.2. Implications of differences between types of gear The general assumption of an average speed of 2.5 knots was confirmed by analysis of VMS data. However, grid trawling, i.e., clean Nephrops trawling, would generally require less speed than fish trawling, and a slight difference in speed between the types of gear was also confirmed by VMS analysis (Fig. 9). This difference gives grid trawling a lower seafloor area swept impact than that of conventional trawling, reducing originally assumed differences.

Fig. 9. Distribution in percent of vessel speed in knots for the two types of gear in the 2–3 knot interval.

Differences in transportation distance assumed in the model did not significantly alter the final results. The higher speed of conventional trawling (Fig. 8) would increase the fuel consumption per effort. Other potential differences, such as, drag resistance and weight, would likely also contribute to grid trawling being more fuel efficient than conventional trawling (Table 3).

Table 3. Likely direction of fuel use if it is not equal between types of gear; + = increase, – = decrease.

Netting1 Depth2 Weight3 Location4

Grid - - - - Conventional + + + +

1 Grid uses a square mesh with better hydrodynamics. 2 Grid is generally used in shallower areas due to optimization of gear performance. 3 Grid has a lower total catch to be hauled. 4 Grid trawling generally occurs closer to the coast.

4. Discussion Grid trawling complies well with management objectives, which are to reduce fishing mortality of cod. However, from a broader perspective, grid trawling has some tradeoffs. Resource use in terms of fuel use per total landings is higher using grid trawls, approximately 1 l extra per kilogram landed, but this inefficiency is less important than the superior protection of threatened species contributed by grid practice. In addition, this study found that discard was highest in the Kattegat grid fishery; however, in terms of susceptibility to impact (VEC) and extent of disturbance (PPR), grid trawling is still superior to conventional trawling. Survival potential is also generally higher for discarded flatfishes and juvenile Nephrops than for the gadoid fish species discarded to a greater extent in conventional trawling. If the impacts are seen per kg of Nephrops landings (after economic allocation), no general elevated fuel use or seafloor impact is seen, suggesting that at present fish stock levels, grid trawling is not generating significant tradeoffs when targeting Nephrops; instead, it has a lower impact on threatened fish species and lower PPR. With the proposed discard ban in the upcoming reform of the EU Common Fisheries Policy, a selective practice such as grid trawling would be preferable, though it is important to be aware of compromises in other areas, such as fuel consumption.

By this study, it was demonstrated that LCA can be used to quantify potential tradeoffs from a management measure and to contrast regional effects (i.e., restoration of locally depleted fish stocks) to potential global effects (such as GHG emissions). Higher resolution of discard impacts was obtained by applying PPR and VEC to the discard mass.

4.1. Implications for fisheries managers Integrated assessments should be carried out to ascertain the likely magnitude of the possible imposed tradeoffs and then determine priorities in order to mitigate the overall impacts of fisheries. LCA could quantify compliance with progress towards a good water quality status by 2020, as mandated by the EU Marine Water Directive [53]. Grid trawling would, in this context, probably be superior to the mixed fishery in terms of threatened species (descriptor 1), depletion of the populations of commercial fish species (descriptor 3), and trophic level distortions (descriptor 4). However, seafloor integrity (descriptor 6) is still relevant to grid trawling (a type of demersal trawling), which is allowed in areas protected from conventional trawling. As muddy habitats are important fishing grounds, they are often difficult to protect due to economic value to fisheries. The trawling intensity of these habitats in coastal areas

54 probably leaves few areas not permanently altered, making the protection of a few areas of biodiversity reserves important for replenishing the disturbed areas. The seafloor impact of grid trawling needs to be further addressed in the future.

The reform of the EU Common Fisheries Policy (CFP) [8] implies that ecology must be a top priority and a prerequisite for other sectors. However, social and economic consequences have traditionally had and will likely continue to have great influence in future CFP versions. Earlier findings have contrasted low GHG emissions from small vessels with high accident risk [54]. The grid construction, according to fishermen, is prone to higher accident risk and may become clogged. Separation of the two trawl practices is only economically viable due to the current large minimum landing size and associated market prices. The question is whether the top priority should be to subsidize selective trawling (to increase profit margin and security on board) or cut fossil fuel subsidies and reduce GHG emissions. It should also be noted that single-species fisheries driven by depletion from formerly fished stocks could incur increasing risks, in terms of both production stability and profits [55]. As present fish stock levels in the area do not allow a sustainable mixed fishery, it could be questioned why the trawling fleet should continue to catch a mainly luxury food item when creeling is an alternative with considerably less associated impact [22].

4.1. Implications for LCA methodology The former LCA study [22] of trawled Nephrops identified higher fuel consumption than was found here. First, a different approach to modeling was used and the system boundaries were set differently; for example, the former study used sample fuel data covering yearly fuel use instead of modeling the whole fleet, aggregated Kattegat and Skagerrak, and using a different definition of the Nephrops fleet. Second, data from all demersal fisheries in Sweden indicate a trend towards decreased fuel consumption of approximately 40% per landing from 2003 to 2008 [56]. In addition, Nephrops catches in 2009 were relatively high at 1334 tons, whereas in 2004 – the year of the earlier study – only 906 tons of Nephrops were landed, leading to relatively high fuel consumption. This indicates limitations of snapshot studies. Earlier findings derived from examining longer periods indicate great between-year differences in pelagic fisheries [57], making different studies difficult to compare. Absolute values for fuel use are not only depending on which approach used, but could also be sensitive to boat sizes in sample data and which transportation scenarios chosen (e.g. speed, length), as it recently was shown that the fuel need derived from this study might be a bit optimistic (Ziegler and Hornborg, in prep.).

This study also demonstrates that accounting only for discard quantity in LCA is a rough measure of impact on the marine ecosystem. Although total discard quantity is high, differences in species composition may imply that the result is not as serious as initially appears. Accordingly, the discard indicators chosen in this study increasingly identify potential environmental effects of fisheries than simply total discard quantity. However, one area of concern for VEC is the divergent perspectives of conservation biology and fisheries management. The lowest decline rate of a species to fall under the IUCN Red List threatened species criteria is a population reduction of 50% in ten years or three generations. The same decline rate could according to management objectives be a fully sustainable exploitation, as

55 the theoretic biomass at maximum sustainable yield (BMSY) is in general at 50% reduction of natural biomass [58]. Possible discrepancies between sustainable natural resource exploitation and adverse effects need to be further addressed in terms of the biological impacts of fisheries, however, congruent assessments from both perspectives have been found in the area of study (Hornborg et al., in prep). In terms of the PPR of discards, LCA can provide interesting insights. Trawling for Norway lobster can be compared to salmon aquaculture in terms of acquisition of primary production. Discards acquire 31–260 kg C per kilogram of Nephrops (economic allocation), equivalent to or even higher than the appropriation from feed in salmon culture, i.e., 18–137 kg C per kilogram of live-weight salmon [59]. The results indicate that discard is a hidden cost of fisheries, making use of PPR as a sustainability tool interesting, if cautions are made on which data sources and historical time frame that are used (Hornborg et al., in prep). According to estimated %PPR from landings in relation to availability [60], the North Sea area was found to have a 40% probability of being sustainably fished, making accounting for PPR in fisheries important, though further elaboration of the implications, in terms of impact, of different PPR levels is recommended.

5. Conclusions and future recommendations Species-selective trawling for Nephrops fulfills the objectives for fish by-catch management in the area; however, from a broader perspective, it is more resource intensive than conventional trawling in terms of fuel use and seafloor disturbance per landed seafood kilo. Still, per kg of Nephrops, grid trawling is superior in terms of threatened species affected while being equal in fuel use. Using LCA, the seafood industry can be made more transparent and potential tradeoffs in resource use and environmental impacts can be identified to facilitate improvements and better resource use. Future modeling of the implications of primary production requirements, threatened species impact, and target stock long-term wastage would improve the results.

More data of greater detail are needed to increase the accuracy of assessments. A study linking vessel size and fish mortality in Danish fisheries suggested a logarithmic increase for gear size [61]; this would be interesting to study in greater detail, as no data were available on individual trawl width. Less secrecy regarding fuel consumption in fisheries would also foster improvement.

6. Acknowledgements We wish to thank Katja Ringdahl, Johan Lövgren, Patrik Jonsson, and Rickard Bengtsberg for contributing data. Leif Pihl, Mattias Sköld, and Andreas Emanuelsson made valuable comments on the manuscript. Funding is acknowledged from Swedish Research Council Formas and the European Commission (LC-IMPACT FP7 Grant Agreement 243827).

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Paper II: Use of red listed fish species as indicators for fishing by- catch impact on sensitive species

Sara Hornborgab*, Mikael Svenssonc, Per Nilssonb & Friederike Zieglera a Swedish Institute for Food and Biotechnology, Sustainable Food Production, Sweden b University of Gothenburg, Department of Biological and Environmental Sciences, Sweden c Swedish Species Information Centre, Swedish University of Agricultural Sciences

*Corresponding author: tel. +46-10-5166696 fax +46-31-833782 email: [email protected]

Summary

Fish stock depletion from overexploitation cause concern not only to fisheries management, but also to conservation biologists and consumers of seafood products. Unintentional catches is one problematic issue that is of great importance to sustainable resource use, and there is a need to have a framework for grasping this information for consumers and fisheries managers. The Swedish national red list for marine fish was evaluated in terms of robustness and possible use for communication and management in a case study of Swedish demersal fisheries in the Kattegat and Skagerrak area. It was found that the national red list showed high consistency with scientific advice and identified traits sensitive to fishing, assessing a much greater part of the species affected by fishing than fisheries authorities do. By further evaluating the varied amounts of red listed fish species occurring in separate fishing segments, it was found that this approach is promising as a carrier of information to differentiate between seafood products in terms of impact on overexploited and sensitive fish species. Increased coverage of the global red list, or more national initiatives, is however important to make comparative studies.

Keywords IUCN, fisheries management, discard Introduction

Current fisheries management has been shown to be insufficient in fully protecting fish stocks from depletion (Hutchings, 2000; Christensen et al., 2003; Myers & Worm, 2003). Species with e.g. limited geographical distribution and specific spawning grounds have been shown to be sensitive to directed fisheries and habitat destruction (Roberts & Hawkins, 1999). It has also been difficult to find solutions for efficient management of highly migratory species (Collette et al., 2011). Single stock management generally also fails to incorporate possible effects on fish species that are unintentionally caught (Brander, 1981; Kelleher, 2005) and many species, in particular by-catch, lack robust reference points for managers to set proper exploitation levels (Davies et al., 2009; ICES, 2009).

The need to monitor and ease fishing pressure on species at risk from fisheries is of increasing concern to managers. The observed problems with current single-species fisheries management have led to the promotion of Ecosystem-Based Fisheries Management (EBFM), a framework that would require managers not only to focus on target stocks, but also on conservation of marine biodiversity (Pikitch et al., 2004) with a range of potential indicators suggested for this purpose (ICES, 2005). Complementing initiatives have also been made, such as the Convention of Biological Diversity (CBD), which recognizes two operational indicators for monitoring global biodiversity trends caused by fishing impacts (Biodiversity Indicators Partnership, 2010), one being the Red List Index (RLI). The RLI is based on assessments made from the International Union for Conservation of Nature (IUCN), which has implemented a red list framework with the aim to categorize species by their relative level of threat to extinction (IUCN Standards and Petitions Subcommittee, 2010). The original idea to ―identify and document those species most in need of conservation attention if global extinction rates are to be reduced‖, has from this been expanded into monitoring trends of global levels of biodiversity loss, with the global outlook as guiding principle of conservation priorities that should be set at the regional level (iucnredlist.org).

Parallel to the movement towards EBFM and setting biodiversity targets, consumer awareness calls for increased information of the environmental impact a seafood product, creating demand for environmental assessments such as life cycle assessment (LCA). Interest in easy- to-grasp information such as eco-labeling is increasing (FAO, 2010), and they are recommended to be based on holistic approaches such as LCA (ISO, 2006), even if this is not always the case. Examples of eco-labels used in the seafood sector are Marine Stewardship Council (MSC; msc.org ) and the Swedish KRAV (krav.se) (Thrane et al., 2009). Unfortunately, there is a general lack of methods to assign impact on species sensitive to fishing from a specific seafood product within the LCA framework (Pelletier et al., 2006), which is of concern in order to avoid to miss out on important aspects due to lack of methods. The impact on Endangered, Threatened or Protected species (ETP) is used by MSC, but the criteria are vague for which species that fall within the category (MSC, 2011).

Fishing policies are not always considering the IUCN red listing of an exploited species (Fiskeriverket, 2010), which could originate from the fact that conservation biology and fisheries management have traditionally been seen as antagonists (Mace & Hudson, 1999). Whereas fisheries managers traditionally focus on single-species assessments aiming at maximum sustainable yield (MSY), conservation biologists, on the other hand, are concerned with extinction risks. Interestingly, the same target for biomass BMSY, i. e. a 50 % reduction of virgin biomass is generally considered to produce MSY – and is the lowest decline rate for being classified as threatened by the IUCN criteria (IUCN, 2010; Reynolds et al., 2005). Fisheries management and conservation biology is then by the motive of their assessments split in two fields, with a fine line in between. In addition to this, red listing of species have been mistrusted (Possingham et al., 2002), possibly from prevailing false perceptions that the assessments are made by ―expert opinions‖ instead of the now revised form with global standards (Rodrigues et al., 2006). Even if it has been found that the decline rate criteria is a useful indicator of population status and consistent with existing management advice in

61 fisheries (Dulvy et al., 2005), red listing of fish species has so far had minor effects on e.g. fishing policies.

A robust framework for assessing fishing impacts on vulnerable fish species is needed from both the manager‘s, practitioner‘s and consumer‘s perspective. In this study, the aim is twofold. First, it is attempted to evaluate the consistency and robustness of the present IUCN red list of marine fish species. This is done by evaluating the national red list in Sweden in relation to fisheries management advices, in addition to life history traits known to be sensitive to fishing pressure (and thus should require attention in a data limited situations). Secondly, to evaluate the outcome of discard composition in Swedish demersal fisheries in ICES area IIIa (Kattegat and Skagerrak) in terms of amount of red listed fish species present. The results are discussed in the context of an operational indicator for fisheries managers as well as product related information schemes. Based on identified limitations for the IUCN criteria, suggestions on modifications to the criteria are also discussed. By this, the intention is to form a base for discussion of the prospects of using indicators such as quantifying red listed fish species in discards, either as a framework within fisheries management, or as a complement to environmental assessments of seafood products.

Material and methods

Methods

The present national red listing of Swedish fish species (Gärdenfors et al., 2010) was evaluated in relation to other assessments of vulnerability (Table 1). The scientific community has identified traits that in general can be considered to make a fish species more sensitive to fishing pressure, such as e.g. large body size, late onset of reproduction and long life span (Jennings et al., 1998; Roberts & Hawkins, 1999). Species with these traits are likely to occur in categories of increased threat status, as well as in dire need to be taken special consideration of in fisheries management when data for proper stock assessments are too scarce. Life history traits for species assessed in this study came from mean values of literature stated in Supplementary material, table 1.

The advice from fisheries managers are in this study considered to be the accurate perception of the stock, even if there is an ongoing discussion on whether this is the case (Worm et al., 2009). The scientific advice was in this study based onthe International Council for Exploration of the Seas (ICES) assessments of the state of the spawning stock biomass (SSB) (ICES, 2009; for detailed information see Supplementary material table 3). Species with a national fishing restriction are listed in Supplementary material, table 2.

Table 1. Assessment methods used to evaluate current IUCN classifications of Swedish fish species; references for each trait are studies supporting the choice of parameter.

Assessment method Comment ICES advice for 2010 Stock advices on spawning stock biomass (SSB) state (Dulvy et al., 2005) Global IUCN classification Status for the species assessed on a global scale

Lmax Maximum length (Jennings et al., 1998; Piet & Jennings, 2005; Greenstreet & Rogers, 2006)

Amat Age at maturity (Jennings et al., 1998; Robert & Hawkins, 1999) Amax Maximum life span (Roberts & Hawkins, 1999)

Only species reproducing in Sweden can be considered for red listing at the national level (Gärdenfors et al., 2010). Even though the Swedish Exclusive Economic Zone (EEZ) can be considered as a part of the North Sea, only national data have been used for the national red list when assessing population trends, Extent of Occurrence (EOO) and Area of Occupancy (AOO). Important population size/trend data include landing statistics, data from the International Bottom Trawl Survey (IBTS) and the Baltic International Trawl Survey (BITS) together with regional and local inventories. Assessments were made by an expert group following a standardized procedure (Gärdenfors et al., 2010) using the best data available for every species. The Swedish Red List has been updated according to IUCN criteria (as accepted in 1994, IUCN, 2010) in 2000, 2005 and 2010. The 2010 Red List is based on data available up until 2009.

To test for relationship between life history traits and red list category, a randomization test on correlation was used, calculated with the software package "Resampling" (Howell, 2007). The ranking was according to the RLI weighting, with LC=1, NT=0.8, VU= 0.6, EN= 0.4, CR= 0.2 and RE=0.

In the case study, threatened species (VEC; i.e. Vulnerable, Endangered or Critically Endangered) in discards from demersal trawl segments targeting certain species on the Swedish west coast was evaluated in terms of quantity as well as in terms of RLI relative ecosystem state of RLI in terms of all marine fish. The RLI is a dimensionless indicator suggested as a measure of progress towards conservation goals (Bubb et al., 2009), where the RLI for all marine fish species in Sweden is assumed to be representing ecosystem state. RLI is calculated as follows:

∑

where Wc(t,s) is the weighting of category c for species s at time t, WEX the weighting for Extinct, and N the number of assessed species excluding Data Deficient (DD) species in the time period and those considered to be Extinct in the initial assessment year. In regional assessments WRE, the weighting for Regionally Extinct, is used instead of WEX. As RLI has been proposed to be able to indicate changes within species complex (Butchart et al., 2005), it is in this study estimated and tested for use to compare discard composition of threatened species from different métiers.

Data sources

Values for max age (Amax), age for maturity (Amat) and max length (Lmax) came from mean values from literature stated in Supplementary material, table 1. Data on trawl discard composition was provided from onboard observer programs. Discards were analyzed per fishing fleet (figure 1).

Grid Pandalus Conventional

ICES IIIa Demersal trawl Grid Nephrops Conventional Fish

Figure 1. Demersal trawling segments in ICES area IIIa with specific discard sampling used in this study. Grid implies species selective trawling. The numbers of hauls were: Pandalus without grid n=25, with grid n=18; Nephrops without grid n=49, with grid n=44; and mixed demersal fish n=31.

For each haul in respective métier, the mass as well as individuals of discarded threatened fish species (VEC) was assessed per kilogram of total landing as well as RLI values. While it has been found that the proportions of threatened invertebrates vary between different trawling segments in the area (Ottosson, 2008), they are presently insufficiently monitored in the observer programs to be evaluated in this respect.

Results

Robustness of red list assessments

Ninety-nine fish species were assessed by the national red list according to the criteria set, such as known reproduction within Swedish waters (data from the Swedish Species Information Centre). Of the assessed species, only three species were classed as Data Deficient (DD). Two species were considered to be Regionally Extinct and 17 were found to be Threatened (Table 2).

The global extinction risk was in general found to be one or two levels lower than the regional extinction risk. The national red list status showed in relation to the global list consistency with 5 species and 7 had a higher level of threat (6 were Not Evaluated globally (NE)).

Table 2. Marine fish species on the Swedish red list of threatened species in 2010. The categories used are Regionally Extinct (RE), Critically Endangered (CR), Endangered (EN), Vulnerable (VU). Definitions of criteria are found in IUCN Standards and Petitions Subcommittee (2010).

Scientific name Common name Nat Criteria for Global IUCN Criteria for global red listing IUCN national red listing listing listing Dipturus batis Blue skate RE CR A2bcde+4bcd (2001)

Acipenser oxyrinchus Atlantic sturgeon RE CR A2d (2001)

Lamna nasus Porbeagle CR A2bd; C1; D VU (CR) VU A2bd+3d+4bd (CR A2bcd+3d+4bd, Northeast Atlantic subpopulation) (2001) Cetorhinus maximus Basking shark CR A2abd; C1; D EN A2ad (2001) Squalus acanthias Picked dogfish CR A2bd VU (CR) VU A2bd+3bd+4bd (CR A2bd+3bd+4bd, Northeast Atlantic subpopulation) (2001) Anguilla anguilla European eel CR A4bcde CR A2bd+4bd (2001)

Pollachius pollachius Pollack CR A2bd; B1ab(i,ii,iv,v) NE Chimaera monstrosa Rabbit fish EN B1ab(v) NT (2001)

Raja clavata Thornback ray EN A2bd NT (2001)

Coryphaenoides Roundnose grenadier EN A2d NE rupestris

Molva molva Ling EN A2bd NE

Gadus morhua Atlantic cod EN A2abcd VU A1bd (1994)

Melanogrammus Haddock EN B1ac(iv)+2ac(iv) VU A1d+2d (1994) aeglefinus

Anarhichas lupus Atlantic wolffish EN A2bd NE

Hippoglossus Atlantic halibut EN A2bc; B1ab(iii,v)+ EN A1d (2001) hippoglossus 2ab(iii,v); C1+2a(i,ii) Galeorhinus galeus Tope shark VU A2d; C1 VU A2bd+3d+4bd (2001)

Somniosus Greenland shark VU D1 NT microcephalus Etmopterus spinax Velvet belly VU A2bd+3bd+4bd NE

Merlangius merlangus Whiting VU A2abd NE

ICES advice for species occurring within the Swedish EEZ covers 30 species (or 39 stocks) in total (see Supplementary material, table 3). Of these species, 22 were applicable for national red listing according to existing criteria, which means that ICES provide advice for 22% of the species that were assessed by the IUCN national framework, as not all species are of interest to fisheries. These 22 species were managed as 31 stocks. For many of the species with a quota, no clear reference points were established and these could thus not be evaluated from an ICES perspective as sustainably exploited or not (listed as uncertain in Table 3). The term ―miss‖ is used to imply failure of the red list to include the species as threatened; a ―false

65 alarm‖ is a species on the red list but not perceived to be at risk by fisheries management (sensu Dulvy et al., 2005).

Table 3. Red list status compared to ICES advice (see Supplementary material, table 3); Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Near Threatened (NT), Least Concern (LC) and Not Applicable (NA).

IUCN ICES n w ICES advice Comment CR Fully consistent 4 species EN 2 false alarm 4 species, 7 stocks Haddocka and codb (Eastern Baltic, stock 25-32). VU uncertain 1 species NT - - LC 3 hits 13 species, 19 stocks Herringc (stock IIIa, autumn 2 miss spawners) and salmond. 14 uncertain NA 8 species aAccording to the Swedish Board of Fisheries, the local stocks in the Kattegat and Skagerrak are depleted (Fiskeriverket, 2010). bStock status has improved in recent years, now considered to be sustainably fished and is KRAV-certified. cIncreased risk to SSB level. dSSB considered to be low.

The comparison of data on Amax, Amat and Lmax to the different categories of threat, showed consistent for results for all parameters. There was a strong negative relationship between all three traits sensitive to fishing and red list category (Amat: R=-0.749, n=73 P<0.0001; Amax: R=-0.646, n=75, P<0.0001; and Lmax: R=-0.606, n=94 P<0.0001, Randomization test of correlation). This implies that fish species with later onset of maturity, longer life span and larger final size are listed in IUCN red list categories at progressively higher levels of threat (Fig 2abc).

Figure 2abc. Mean values for Swedish marine fish species occuring in the different national threat categories, with a) maximum life span b) age for maturity; c) maximum size.

Management application The RLI index for marine fish species shows a slight negative trend in Sweden during the last fifteen years (-0.0004, R2=0.4194). RLI for different discard compositions differed between fishing segments, with discards in the mixed fish trawl métier having the highest amount of threatened fish species in the discards (that is the lowest RLI value, as if no of red listed species would be present, this result in a value of 1, Fig 3a). In terms of mass of threatened fish species (VEC) discarded per kilogram of landing, the conventional trawl fishery for Nephrops has the highest proportion (three individuals or 0.3 kg per landed kg) whereas grid trawling for Pandalus showed the lowest among the studied trawl fisheries (Figure 3b). Haddock, whiting and cod were in general the most abundant in both mass and numbers, in the Pandalus fishery also Rabbitfish.

Fig. 3. a) RLI (with standard error) for discards in different fishing métiers. General RLI value for all marine fish species in the area for 2010 was 0,87 (dotted line) and optimum value for RLI is 1 (bold line); b) VEC, discards of threatened species in mass (kg) per kilo of total landings with SD and c) same as b but as individuals.

Discussion The fish species occurring in the different categories of threat on the Swedish national red list showed high consistency with general perceptions of fish having sensitive traits to fishing pressure, mean values for Amax, Lmax, Amat of fish classified in different categories of threat was increasingly higher with increasing level of threat. Management perceptions also showed high correlation with conservation interests, with red listed species rarely being considered as sustainably exploited, consistent with former findings (Dulvy et al., 2005), however with discrepancies at stock level such as for Eastern Baltic cod. Noteworthy, although the area is well monitored, only 30 of the 99 fish species assessed by the IUCN were at all considered by ICES. This is due to the fact that not all species are targeted, and indicate the complementarity between ICES and IUCN for assessing fishing impact from by-catch and discard. Of the 17 threatened species, 10 were assessed by Swedish fisheries managers, all species generally in line with the red list perception given that proper management is enforced (Fiskeriverket, 2010). Given the more extensive coverage of the red list, this makes this framework useful as carriers for aggregated information of fish species sensitivity to fishing, and could hereby act as a complement to stock assessments in data scarce situations on abundance trend coupled with sensitive traits in line with EBFM.

The intent of the red list is to provide an alarm signal when a decline is observed for an unmanaged species (Mace & Hudson, 1999), whereas managed stocks on the other hand, have a completely different data situation and are more regulated, ideally accordingly protected by management. By-catch fish species on the other hand benefit more from increased management considerations. In this study it has been shown that several of the targeted species, hence considered as ―managed‖, have no conclusive fisheries advice due to data

68 deficiency. As fisheries management is supposed to take account of fishing mortality on by- catch of vulnerable species (ICES advice, 2008), it would then be desirable not only to cover charismatic species, e.g. dolphins, but to include threatened fish species as well, ideally also invertebrates. Numerous ways of estimating by-catch vulnerability have been suggested (e.g. Pope et al., 2000). Utilizing the red list framework on fish species with insufficient stock assessments, effort restrictions and gear promotions could be further guided by the differentiated impacts imposed by various discarding practices on fish species outside the management framework (Hornborg et al., 2012).

RLI has before been suggested as a good indicator for biodiversity targets (Brooks et al., 2004). It provides a diversity measure without mass dimension, as it is based on the number of threatened species present without considering relative abundance. This makes it likely to be sensitive to a sampling effect, when an infinite number of samples will eventually lead to the same results for all discard compositions, as the species count is not taking into account the amount. On the other hand, this study showed to have less variation in RLI between hauls than gauging VEC species per landed kg. Stating VEC (as individuals or mass) per landed kg, the quantity in relation to landings is provided, but with greater uncertainties. Mixed demersal fish trawling was shown to be of greatest concern with regard to RLI, i.e. a higher number of red listed species is present in each haul, which is not surprising as this métier is targeting fish of which many are severely depleted. However, mixed trawling targeting more Nephrops was of greatest concern to VEC (mass and number). The high VEC values are derived from great amounts of quota-filled fish species discarded, in combination with a higher discard rate relative landing. Species-selective trawling for Nephrops, had the best RLI value, however not lowest VEC due to greater quantities of juvenile whiting discarded as well as having a higher discard rate in relation to landings in relation to cleaner fish trawling. As for assessing impact on sensitive species in environmental impact assessments of seafood production, kg or number of VEC fish species per landing would probably be the most illustrative and easily interpreted choice, however the great uncertainties requires a great number of sampled hauls. Due to the un-intuitive optimum value of 1 for RLI when red listed species are absent, for facilitated communication, the order of weighting should preferable be reversed, i.e. a value of 0 should indicate that no red listed species affected.

The VEC approach to discard impact attributed to a seafood product could capture sensitive fish species, but will still miss out on invertebrates due to insufficient monitoring. To further complement the assessment of impact on sensitive species from a seafood product, improved monitoring of invertebrates must be put further up on the agenda. Deep-sea trawling is for example likely to degrade sensitive ecosystems dominated by invertebrates (Roberts et al., 2006). Unfortunately, an alarm in terms of VEC or RLI would fail to set off even for equally sensitive fish species in this case, as the IUCN is not sufficiently covering deep sea fish species (Devine et al., 2006). However, classifying different discard impacts from fisheries merely by amount or relative a global discard rate, and not differentiating between the varied sensitivity to the imposed impact from different species compositions, will make deep sea fisheries appear as favorable from a discard perspective (Vázquez-Rowe et al., 2012). With increasing coverage by the IUCN, this problem will hopefully diminish.

As the global red list at present covers all cartilaginous fishes but not even 5 % of the globally described bony fish species (Hoffman et al., 2010), the national red listing in Sweden was the most comprehensive classification to use in for this study (Table 2). However, due to the red list criteria set on reproduction within the country‘s borders, several sensitive species in Swedish marine capture fisheries were missed. Even so, the IUCN approach covered more species than the fisheries management framework did. When deciding on which level of assessment to use, global or national, it should be noted that only fish stocks, rarely fish species, are under real threat of true extinction (Reynolds et al., 2005), fish stocks rather than species might be more ideal for the global IUCN red list. To conclude, the preferred geographical resolution needs to be further discussed within the IUCN framework as well as in seafood assessments of impact on sensitive fish species by LCA.

In Sweden, there is an additional national legislation for protecting species by landing prohibition that cover six of the red listed species as well as some species non-applicable to the national list (FIFS 2004:36; see Supplementary material, table 2). One of the species not applicable for a national red list but with a regional landing prohibition, is Atlantic Bluefin tuna (Thunnus thynnus). Atlantic bluefin tuna peaked in landings in Swedish waters in 1942, with declining catches up until 1991. Now it is considered to be completely extinct in the area. This species is not known to ever have been reproducing in Swedish waters, thus not applicable for national red listing at a national level. However, due to unsustainable fishing pressure, the local occurrence has been severely decreased. The question is how the national red list best deal with highly migratory species in relation to national conservation plans, regionally extinct or not applicable? Both global and national red list status could be of importance, especially for highly migratory species such as many marine fish species. Globally, the species is considered to be Endangered (IUCN, 2011). It has been suggested that red lists at national levels are needed for conservation authorities and have been shown to be generally satisfying in consistency with global assessments (Gärdenfors, 2001). In this study, global versus national listings had a tendency to state somewhat higher level of threat at a national level, which is not surprising as fish species are of a lesser threat to extinction than local stocks (Reynolds et al., 2005). It is also likely that within a fish species as well as within a managed ―stock‖, there could be many genetically distinct populations of importance to consider (Nielsen et al., 2009; Svedäng et al., 2010).

On land, the occurrence of threatened species in an area can cause changes in development plans for human activities. Fisheries are presently targeting species at the same level of threat as Pandas (EN) and Orangutangs (CR) (IUCN, 2011).This downward trend might be reversible if a stricter management regime was in place earlier. As an example, the European eel, Anguilla anguilla (CR; IUCN, 2011), is now recognized as belonging to Appendix II on the much more constraining Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) list (CITES, 2011), yet the species is still being exploited commercially. This implies that if no further efforts are made, the species could end up on Appendix I which would prohibit international trade. As the red list recognizes several other species at the same level as the eel, strengthening the position of the red list in society by

70 giving red lists of fish species more notice could contribute to avoiding more fish species ending up on the CITES list.

Conclusions

 The national red list in Sweden was shown to be consistent with other criteria set for vulnerable species in need of protection, like scientific advice and life history traits.  Stating VEC per seafood product landed would additionally enhance product related environmental assessments of seafood, e.g. LCA‘s. Increased coverage of species assessed is encouraged for comparative studies.  To fisheries management, the red list could provide early warning signals for species that are by-catch, when no advice and hence sufficient management regime is in place.  If VEC would be estimated per quota allowance, it could serve as guidance to fisheries management to protect less protected species and a movement towards Ecosystem Based Fisheries Management.  Red list assessments of fish species might prove to be more suitable at stock level.

Acknowledgements

We wish to thank the Swedish Research Council Formas and the European Commission (LC- IMPACT FP7 Grant Agreement 243827). Also, thanks to Katja Ringdahl for providing discard data; Daniel Valentinsson and Andreas Emanuelsson for contributing in discussions.

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SUPPLEMENTARY MATERIAL

Table 1. Mean values for all literature below was used for life history traits.

Author Titel Aschehoug, Pethon P. Aschehougs store fiskebok Curry-Lindahl, Kai Våra fiskar FishBase Species information at fishbase.org Wheeler Key to the Fishes of Northern Europe Kottelat, Maurice & Freyhot, Jörg Handbook of European Freshwater fishes IUCN Species fact sheet at iucnredlist.org

Table 2. Fish species under local fishing regulation prohibiting landing of the species (FIFS, 2004).

Scientific name Common name National red list status Pelecus cultratus Sichel NA Petromyzon marinus Sea lamprey NT Squalus acanthias Picked dogfish CR Scyliorhinus canicula Small-spotted catshark LC Cetorhinus maximus Basking shark CR Lamna nasus Porbeagle CR Dipturus batis Blue skate RE Raja clavata Thornback ray EN Alosa alosa Allis shad NA Alosa fallax Twaite shad NA Thunnus thynnus Atlantic bluefin tuna NA Anguilla anguilla European eel CR

Table 3. IUCN listing in relation to ICES advice. The categories are Regionally Extinct (RE), Critically Endangered (CR), Endangered (EN), Vulnerable (VU), Least Concern (LC), Data Deficient (DD) and Not Applicable (NA). Hit implies fisheries management and the red list agreeing; miss is a failure by the red list to identify species at risk, false alarm is the red listing of a fish species considered to be sustainably exploited.

Species Stock IUCN SSBpa Fpa F long F long Hit Miss False Un- yield target alarm certain Argentines NA No NA expansions Basking CR 0 0 0 0 1 shark Blue ling NA No directed NA fisheries Blue whiting NA Full Harvested Overfished Above NA reproductive sustainably capacity Brill 22-32 LC Unknown Unknown Unknown No target 1 Cod 22-24 EN Increased risk Undefined Over- Above 1 exploited 25-32 EN Undefined Sustainable Appropriate Below 1 Kattegat EN Reduced Unknown Unknown Unknown 1 reproductive capacity Skagerra EN Reduced Increased risk Overfished Above 1 k reproductive capacity Dab LC Unknown Unknown Unknown No target 1 European CR 0 0 0 0 1 eel Flounder 1 LC Unknown Unknown Unknown No target 1 Greater NA No NA forkbeard expansions Haddock IIIaN EN Full Harvested Appropriate Below 1 reproductive sustainably capacity Hake IIIa NA Full Harvested Overfished Appropriate NA reproductive sustainably capacity Herring IIIa (spr), LC Undefined Undefined Overfished 1 22-24 IIIa (aut) LC Increased risk Harvested Overfished Above 1 sustainably 25-29 LC Undefined Increased risk Over- No target 1 exploited 30 LC Undefined Sustainable Appropriate No target 1 31 LC No - - - 1 assessment Horse NS NA Unknown Unknown Unknown - NA mackerel Ling 1 EN CPUE 1 reduced level Mackerel NS LC Full Increased risk Overfished Above 1 reproductive capacity Norway NS NA Full Undefined Undefined NA pout reproductive capacity Plaice Baltic LC Unknown Unknown Unknown No target 1 IIIa LC Unknown Unknown Unknown No target 1 Porbeagle 1 CR 0 0 0 0 1 Roundnose IIIa EN No expansion 1

76 grenadier Salmon 1 LC Low No target 1 Saithe IIIa LC Full Harvested Appropriate Appropriate 1 reproductive sustainably capacity Sandeel IIIa LC No - - - 1 assessment Sea trout 1 LC - No target 1 Sole IIIa LC Full Harvested Appropriate 1 reproductive sustainably capacity Sprat 22-32 LC Undefined At risk Over- No target 1 exploited IIIa LC No advice for - 1 TAC Spurdog 1 CR 0 0 0 0 1 Turbot 22-32 LC Unknown Unknown Unknown No target 1 Tusk NA CPUE NA reduced level Whiting IIIa VU Unknown Unknown Over- No target 1 exploited

Paper III: Mean Trophic Level and Primary Production Required in Swedish fisheries over a century: prospects and limitations of the indicators

Sara Hornborgab*, Andrea Belgranoc, Valerio Bartolinocd, Daniel Valentinssonc & Friederike Zieglera. a Swedish Institute for Food and Biotechnology, Sustainable Food Production, Sweden b University of Gothenburg, Department of Biological and Environmental Sciences, Sweden c Swedish University of Agricultural Sciences, Department of Aquatic Resources, Institute of Marine Research, Sweden d University of Gothenburg, Department of Earth Sciences, Sweden

*Corresponding author: tel. +46-10-5166696 fax +46-31-833782 email: [email protected]

Summary

Trophic indicators such as mean trophic level and primary production required from fisheries are increasingly used to describe the sustainability of fisheries exploitation. This article discuss limitations to current use, as well as suggesting new approaches based on results from a case study of Swedish fisheries, using data on landings and discards, surveys and primary production levels in the Kattegat and Skagerrak area during the past century. It was shown that it is important to be aware of the importance of the quality of the data used, in particular the level of detail, and to use the appropriate historic time frame in order to better interpret results. Further studies on trophic level changes and transfer efficiencies in regionalized case studies are also recommended in order to compare the sustainability of different fishing practices.

Keywords: MTL, PPR, sustainable fisheries

1. Introduction Fisheries have been known to cause trophic distortions in marine ecosystems (Christensen et al., 2003, McClenachan et al., 2008). It is of great importance for fisheries sustainability and productivity to e.g. identify the risk of trophic cascades following species loss (Casini et al., 2009) as well as understanding the impact from overexploitation of top predators for the resilience of ecosystems (Baum & Worm, 2009). The processes generating the trophic structures of ecosystems and their function have been intensely studied in relation to the vulnerability to perturbations by e. g. looking at the role of bottom-up versus top-down processes in controlling the structure and dynamics of ecosystems and food webs (McCann, 2012; Frank et al., 2006). Although there are no conclusive findings yet, indicators related to trophic levels of species and their position in the food web are currently used to quantify fishing trophic impacts.

One of the most renowned trophic indicators is the estimate of mean trophic level (MTL) in landings. By monitoring changes in MTL, it has been suggested that depletion of top predators due to fishing pressure will result in a decline in MTL. After a decline in MTL derived from a suggested ―fishing down the food web‖ was illustrated in global landings statistics (Pauly et al., 1998), MTL as an indicator attracted great attention and the concept is now considered by the Convention of Biological Diversity (CBD), to be ―ready for global use‖ as Mean Trophic Index, MTI (2010 Biodiversity Indicators Partnership, 2010). It is in addition stated that ―the concept and approach is now widely accepted‖. There are however unsolved issues with this indicator regarding the possibility to capture true trophic distortions from exploitation patterns. When reexamining global MTL data, Essington et al. (2006) instead identified an increase in MTL, only by increased landings of low trophic level species, MTL was negatively affected, commonly called ―fishing though marine food webs‖. Furthermore, it was recently shown that MTL from landings may differ from MTL from fisheries independent data such as scientific surveys (Branch et al., 2010). In addition to this, the original perception that higher market values trigger depletion of top predators was recently dismissed by Sethi et al. (2010); no correlation with high trophic level and high prices could be seen.

Another trophic indicator related to the MTL concept is the Primary Production Required (PPR) from landings (Pauly & Christensen, 1995). PPR is an estimate of the magnitude of primary production needed to produce one kilogram of a species at a certain trophic level. Exploiting species at a lower trophic levels results in lower PPR values, which may be interpreted as lower ecosystem costs, and PPR per landing has been suggested to be a currency to ―compare the ecological cost of fishing among different time periods or systems‖ (ICES, 2005). As it in recent years has been suggested that present biomass removal from fisheries in relation to ecosystem production cause ecosystem overfishing, and reducing PPR, that is proportionally increasing fishing at lower trophic levels or reducing overall landing quantity, is required to increase the sustainability of marine fisheries (Coll et al., 2008; Chassot et al., 2010; Swartz et al., 2010). PPR is additionally used as an environmental impact category in seafood production to differentiate between biological resource use of different seafood production systems as ―Biotic Resource Use‖ (e.g. Papatryphon et al., 2004; Pelletier et al., 2009; Hornborg et al., 2012). In addition, a combination of PPR and MTL values has also been used to form a measure of the level of ecosystem exploitation (Tudela et al., 2005; Libralato et al., 2008).

Clearly, trophic related indicators are presently used and are of importance, but the quest to capture true trophic level distortions derived from fishing impacts as well as the interpretation of the results is challenging. The aftermath of ―fishing down marine food webs‖ (Pauly et al., 1998) highlight the need for further evaluations of the MTL indicator. Instead of dismissing the whole concept of fishing down the food web (Hilborn, 2011), increased insight is needed on how trophic indicators properly can be used, interpreted and possibly revised. It has before been suggested to evaluate MTL in more regionalized studies (Caddy et al., 1998; Stergiou & Tsikliras, 2011), and applications of trophic indicators in different marine ecosystems are will contribute to evaluate their suitability for indicators that could be used to an ecosystem

79 approach to fisheries, as different ecosystems have different trophic transfer dynamics (Cury et al., 2005; Frank et al., 2007; Conti & Scardi, 2010).

The aim of this study is to illustrate and present some of the potential limitations of aggregated MTL and PPR trends, and to discuss further perspectives. Changes in MTL and PPR were studied in historical landing data covering over a century of Swedish fisheries in the Kattegat and Skagerrak (ICES area IIIa). This data is compared to scientific surveys, discard monitoring as well as historic levels of available primary production. The discards are studied at the level of specific fishing segments, and the historical timeframe is extended further than in previous studies (e.g. Pauly et al., 1998). In the light of the reformed Common Fisheries Policy of the EU, which promotes selective gears as well as a move towards an ecosystem based approach to fisheries management (CEC, 2008; CEC, 2009), concerns with expressing the need to reduce the PPR of fisheries as well as the effect on global MTL trends are discussed, as well as prospects for using trophic indicators to consumer related communication of seafood products.

2. Material and methods Landing compositions were studied from data compiled by the International Council for Exploration of the Seas (ICES), covering Swedish landings during 1903-2010 from the Kattegat and the Skagerrak (ICES area IIIa). During 1962-1974 landings from this area were not separated from the North Sea (ICES areas IVb+c) and were therefore excluded. Trophic level (TL) estimates of fish species were taken from FishBase (fishbase.org) and for invertebrates from SeaAroundUs (seaaroundus.org). Primary Production Required of landings was estimated as:

PPR=∑ ⁄

with landings yield Yi for species i with trophic level TLi and a transfer efficiency between trophic levels of 14 % used for the studied area (Coll et al., 2008; Libralato et al., 2008; Link, J.S., pers. comm.), assuming that there have been no changes in either TL or TE during the studied period. By dividing the total amount of PPR by the amount of landings, PPR per landing was evaluated over time.

Mean Trophic Level of landings was estimated as follows:

MTL=∑

for each year where TL and Y are the trophic level and the yield for species i.

Landing components with insufficient species identification were excluded from PPR and MTL estimates (an average of approximately 2 %, if excluding some extreme years predominantly in the 1950s with levels around 20 %). For unspecified sharks, rays and skates a default value of 3.7 was used (Pauly & Christensen, 1995).

Scientific survey data came from the International Bottom Trawl Survey in IIIa (IBTS, CPUE from the longest time series, i.e. quarter 1 between 1979-2010).

All 2009 discard data, including both fish and commercial invertebrates, during one year (2009) from the demersal trawl fleet were analyzed by pre-separated targeting segments, sampled by trained scientific observers in accordance with the Data Collection Framework (DCF; EC Council Reg 199/2008). Fisheries total PPR in the area was correlated against data on available primary production (PP) provided by the Swedish Meteorological and Hydrological Institute (www.smhi.se) in the area during 1985-2010 (as mean mC*m2*year) from one station based in the Skagerrak.

3. Results A progressive increase in Swedish landings is observed from the 1920s until the end of the 1990s, followed by a rapid decrease (Fig. 1). Before the 1920s, the records are less reliable in quality and show more fluctuating landings.

Both MTL and PPR reveal wide fluctuations during the 20th century, a negative trend in landings is however seen over the entire time period (MTL: R2= 0.1025; PPR R2=0.0742; Fig. 1 and 2). In shorter time scales, both negative and positive trends can be seen. An initial positive trend of both MTL and landings followed by a generally high MTL; with progressively lower total landings, a shift towards a negative trend of MTL and positive trend of landings occurs; finally resulting in a combined negative trend (see Supplementary material figure 1a-d). The observed variability originates mainly from differences in relative proportion of species at different trophic levels, to a lesser extent from a depletion of higher trophic levels species over time.

Between 1915 and early 1960s, the PPR per landing was generally high. In the mid-1970s, after the 1962-1974 gap in the data, PPR per landing appears to be at lower levels than in the previous period, and a further rapid decrease of PPR per landing (while the volume of landings increased) followed in the 1980s as a result of the increase in herring landings (Fig. 1b). In the last two decades, PPR per landing fluctuated around low levels, with occasional peaks due to high landings of species above TL 4. These are likely the result of unregulated fishing for blue whiting (no agreed TAC for blue whiting pre 1994 and 1997-2005).

Figure 1. (a) Landings in mass per TL and overall MTL per year in Swedish landings (ICES area IIIa), 1962-1974 excluded. Dominating species in TL <2.99 invertebrates; TL 3-3.49 sprat and herring; TL 3.5-4 mackerel; TL >4 gadoids. (b) Landings in mass per TL and PPR/landing per year in the same data set as (a).

The uncertainty of MTL is great due to great standard deviation of TL estimates. However, applying the extreme standard deviation values for TL for herring did not alter the negative trend, only the rate of decline, despite the fact that since 1903, Atlantic herring has contributed with 64 % of accumulated total landings and thus has a great influence on landing MTL. However, excluding herring and sprat and all other species below TL 3.5 from the MTL, no trend can be seen (linear regression, R2=0.0023 after exclusion of outliers during 1903-1906, see Supplementary material figure 2).

Primary production data from the area show that the proportion of available PP utilized by fisheries has been steadily declining (Fig. 3a). However, combining values for MTL and %PPR, would qualify the fisheries as progressively more sustainable; the most recent values have both low %PPR and MTL (Fig. 3b).

Figure 3a) Primary production (PP) in the area (dotted line) and the proportion required from fisheries (%PP) b) %PPR combined with MTL from landing Swedish data seen from relative a general perception on fisheries sustainability adopted from Conti & Scardi (2010).

Most important to recognize is the comparison with landings data and the snapshot analysis of discards from different demersal trawling segments in the area. Great differences were seen in MTL and PPR between landings, discards and catches respectively (Table 1). The studied segments contributed to 19 % of total landings in the area the same year, and were dominated in volume by northern prawn, Pandalus borealis (6%, selective- and conventional trawling combined); 72% of the remaining landing consisted of herring and sprat. Landing PPR of a targeted species was shown to be as low as 29% of total catch PPR when including discards (species selective trawling for Nephrops norvegicus). As the aggregated values for all landings in 2009 were for PPR 36 per kg landing and MTL was 3.32, the increased level of detail illustrates the extent of limitations with using landings data. The divergence of MTL and PPR by métier in relation to total landing MTL is also seen when comparing landings data with survey data; landing MTL showed no correlation with survey MTL during 1979- 2010 (Pearson‘s r= -0.06779).

Table 1. PPR and MTL in landings, discards and catch from 2009 from different trawling segments targeting the listed species. Discard figures are per one kg of landings. Shaded columns are data that will show in landings. Grid refers to species selective trawling.

Targeted species n Kgdisc/Kgland MTLland MTLdisc MTLcatch MTLland/ PPRtarget %PPRtarget

MTLcatch Pandalus borealis 25 0.73±0.40 2.69±0.32 3.15±0.25 2.90±0.25 0.92 3.20 44±28 Pandalus borealis (grid) 18 0.37±0.32 2.46±0.00 2.63±0.21 2.50±0.06 0.98 3.20 61±19 Nephrops norvegicus 49 1.38±0.78 3.36±0.36 3.48±0.32 3.45±0.33 0.97 8.43 42±22 Nephrops norvegicus (grid) 44 1.94±1.01 2.93±0.07 3.19±0.14 3.10±0.12 0.95 8.43 29±18 Mixed demersal fish 31 0.33±0.23 4.22±0.16 3.97±0.19 4.18±0.12 1.01 237±45 83±13 Witch flounder (Glyptocephalus 3 0.33±0.23 4.03±0.07 4.14±0.17 4.14±0.14 0.97 15.34 43±7 cynoglossus)

4. Discussion Mean trophic level of landings is more a gear and targeting pattern effect within a region, thus inadequate to capture large scale and global properties of the ecosystems, but instead is a metric appropriate for small and medium spatial scale studies. The varied results in MTL trend from previous regionalized studies (Pinnegar et al., 2002; Greenstreet & Rogers, 2006)

83 could in part be explained by different regions having different ―back-ground noise‖ (e.g. market demand for certain species, effort allowances on gears and quota restrictions) that are not seen in aggregated figures but highly affect catch composition. This was in this study shown to be especially important for invertebrate fisheries, as catch MTL differs to a greater extent from landing MTL (table 1). Not acknowledging this, only e.g. 5 % of the total PPR to one ton of Pandalus is considered by only studying the Pandalus part of the catch (44% if included all landings within the segment). In the area studied, the selective trawl fishery for Nephrops set off in 2004 from the recovery plan for cod (Madsen & Valentinsson, 2010), a measure taken to mitigate fishing pressure on depleted top predators such as cod from discarding practices. As this fishery contributes to a progressively greater part of the landings, landing MTL decrease as lower amounts of top predators are landed (this would be interpreted as a negative effect on MTL). Still, it protects top predators from overexploitation, which certainly is needed (Catchpole et al., 2007). PPR per landing or MTL as an aggregated global trend does not seem to be a robust indicator of fisheries sustainability. Also of importance to clarify, a decreased MTL of landings (that is not favorable to the CBD) will be the result of decreasing PPR per landing, which is in dire need according to some studies (Chassot et al., 2010; Swartz et al., 2010). This needs to be accounted for in relation to MTL targets.

It was also found that the exclusion of lower trophic level species from the analysis generated no MTL trend. This might in part be explained by the gadoid outburst in the region during the 1960s-1980s, which was considered to environmentally driven (Cushing, 1984). The MTL as an indicator is hereby unable to disentangle the effect of environmental variables from fishing pressure, as it is well-established that most of the higher trophic level species in the area has been severely depleted during the studied time period (Bartolino et al., in press; Cardinale et al., 2011). In the North Sea, changes in size composition of the landings have been found to be more clear than trophic level changes, as well as it could also be argued that the trophic levels attributed to the different species have most likely changed under the studied time period (Jennings et al., 2002). Complementing PPR or MTL in fisheries with trends of vulnerable species, is therefore necessary to capture further depletion of overexploited fish stocks (Hornborg et al., 2012; Hornborg et al., in prep), an important result to environmental system analysis of capture seafood production (e.g. Ramos et al., 2011; Vázquez-Rowe et al., 2012). For fisheries management, the MTL/PPR concepts can be used to assess trophic impacts from different fishing practices (operating in the same area at the same time period) as a move towards Ecosystem Based Fisheries Management.

The historical perspective is also very important. This study showed that before the great expansion of industrialized fisheries post WWII (Hasslöf, 1949), MTL of landings were decreasing in the area, before the first stock collapses attracting attention in the 1960s. This is in line with findings from Coll et al. (2008), as the North Sea was suggested to in terms of PPR being overfished already in the 1950s, but has in recent years shown a slight increase in sustainability due to management efforts. As these results are based on landings in combination with only theoretic discard PPR, the important differences seen in this study between different fishing segments were not accounted for. The variability of the global MTL

84 trend during the last century could also originate from fisheries being in different stages of development; implying that differences between regions must account for the time period of exploitation in the area, which is not possible to account for in aggregated global trends of MTL.

The historical context of PPR values must also be increasingly understood before any conclusions on fisheries impacts on ecosystem production can be made. PPR from landing must be carefully used as an ―ecological footprint‖ as has been suggested in Swartz et al. (2010). This study showed the importance of discard for the total PPR from landings, making quality of data highly relevant. The historical perspective brought on by this study also shows how the rich and highly productive waters of the Kattegat and Skagerrak area are at their all times lowest production in terms of landings, utilizing progressively less of the available primary production, at the same time as %PPR is low. These waters, with historically more diversified food webs, have had a higher total fish production, but have with time been downgraded in terms of ecosystem structure by depletion of top predators, into not being able to capture the increasing primary production, which instead falls through the system and cause hypoxia, which is of concern to fish production (Pihl, 1994; Richardson & Heilmann, 1995; Lindahl et al., 2009). Eutrophication in the area has on the other hand been suggested to have caused an increase in fisheries yield in the 1950s-1970s, but with a shift from dominace of demersal species to pelagic species (Nielsen & Richardsson, 1996).

Last, it should be noted that the values for %PPR from landings found in this study (Fig. 3) are at times a bit high (ranging from 15 % down to 3 % with time), considering that Denmark stands for nearly 70 % of the landings in the area and discards are not included. For the whole North Sea ecosystem, total % PPR from fisheries has been estimated to be 6% (Coll et al., 2008) to 13 % (Libralato et al., 2008). However, the relative values for the historical trend does not alter with changes to absolute values, but illustrates constraints from uncertainties regarding TE with PPR estimates.

5. Conclusions Our study points out the importance to consider available information at the level of specific fishing segments, as well as considering the historical timeframe when developing trophic indices such as the MTL or PPR. Further development of trophic indicators should be made to be able to account for development and changes in the fisheries (e.g. the introduction of more selective gears) such as those proposed by the EU reform of the Common Fishery Policy (CEC 2008; CEC 2009).

There are several questions that should be further addressed by collaborative interdisciplinary initiatives to test the validity and applicability of MTL and PPR as indicators of sustainability. Clearly landing data show great constraints, and it is questionable if this data at all should be used for the intended purpose. Further studies are needed to evaluate the effect of fisheries harvesting in different regions. To accomplish this, further data on how trophic levels and transfer efficiencies may change in time and across different ecosystems and regions are of great value for this.

PPR could possibly be used for Ecosystem Based Fisheries Management and for seafood labeling information, given that the values are based on catch data instead of landings, have the appropriate spatial resolution with regional differences accounted for, are complemented with information on impact on overexploited fish stocks and have an accurate historical perspective.

Acknowledgements This study was funded by the Swedish Research Council Formas and the European Commission under the 7th framework program on environment (ENV.2009.3.3.2.1: LC- IMPACT–Improved Life Cycle Impact Assessment methods (LCIA) for better sustainability assessment of technologies). We also want to thank Katja Ringdahl and Barbara Bland for assisting with discard- and survey data; Per Nilsson, Leif Pihl and Andreas Emanuelsson for contributing in discussions.

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Supplementary material

Figure 1a-d MTL trends during different time periods.

Figure 2 (a) MTL of Swedish landings 1903-2010; (b) MTL of Swedish landings of species above TL 3.5, outliersduring 1903-1906 removed (c) PPR/kg landing.