Cancer Pagurus) in the Kattegat and the Skagerrak – Implications for Sustainable Management

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Fisheries biology of the edible crab (Cancer pagurus) in the Kattegat and the Skagerrak – implications for sustainable management

Anette Ungfors

Doctoral thesis in Marine Ecology 2008

Faculty of Natural Sciences

Department of Marine Ecology-Tjärnö 452 96 Strömstad Sweden

Avhandling för filosofie doktorsexamen i marin ekologi vid Göteborgs universitet. Avhandlingen försvaras offentligt på engelska, enligt beslut av den naturvetenskapliga fakulteten, fredagen den 13 juni 2008 kl. 10.00 i föreläsningssalen på Sven Lovén centrum för marina vetenskaper, Tjärnö-Strömstad.

Examinator: Professor Per Jonsson

Fakultetsopponent: Dr. Julian Addison, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Lowestoft Laboratory, United Kingdom

Published by the Department of Marine Ecology, University of Gothenburg, Sweden

Anette Ungfors, 2008 ISBN: 91-89677-41-2

Cover illustration: The edible crab (Cancer pagurus) by Helena Samuelsson Cartoons: Copyrighted by Mark Parisi, printed with permission. Print: Intellecta Docusys AB, Västra Frölunda 2008

Till mina allra käraste Niclas, Amanda & Malte, Mamma & Pappa

3 4

ABSTRACT: The European edible crab (Cancer pagurus) is exploited to a varying degree in its area of distribution. Landings in United Kingdom and Ireland may have peaked around year 2000, reaching 25 000 and 13 000 tonnes, respectively but have slightly decreased since. On the other hand, landings in Norway have quadrupled in a decade, now reaching 8000 tonnes, which is due to industrial and governmental funding and subsidies, and an increased northward crab distribution. Official commercial landings in Sweden are approx. 150 tonnes. Compared to countries such as UK and Norway the Swedish landings are low but the crab fishery plays an important role for coastal fishermen along the Swedish west coast earning a living from several alternative fisheries through out the year.

The research covered in this thesis is focused on management prerequisites for sustainable exploitation of the edible crab in the Kattegat and in the Skagerrak. I have studied if the present management strategy (escape gaps) is adequate for a sustainable recruitment, and I have also investigated key knowledge for management of commercial stocks, the stock structure. I have also estimated to what degree the stock is exploited and I have performed two independent stock abundance assessments.

I present data (paper I) that describes at what size female and male edible crab reach sexual maturity, based on characters as sperm presence, gonad development and morphometric analyses of abdomen or chela. These data indicated that the present indirect minimum landing size maintained by escape gaps size is not adequate. A minimum landing size for females need to be set to 132 mm to allow 50 % of the individuals to be physiologically mature before being fished. Considering indications that even larger sizes are necessary for spawning, 140 mm CW is a more appropriate MLS to strengthen the spawning stock. Males were shown to mature at smaller sizes as 50 % of the males were mature at 120 mm CW. Furthermore small males, despite being physiologically mature, might not have the same chance for copulation as larger males. For practical purposes, in addition to the copulation advantage of larger males, 140 mm CW is the recommended MLS also for males. Therefore the escape gap size needs to be increased to 90 mm, from present 75 mm.

Together with colleagues in paper II I have looked at the migration potential, using mark- recapture technique of the crab along the Swedish west coast, as an indication of stock structure. The potential for crabs to move between geographical areas, is one component of the connectivity between areas, and a high migration potential indicates high connectivity which may lead to wide stock distributions and no distinct stock structure. Our study showed a high propensity for migration among females which in many cases moved distances of 100 km, or even as far as 228 km whereas males most often were found within shorter distances from the release point also after several years. The direction of the long-distance female migrations >20 km was predominately towards the south. This southward migration of females may compensate for the northward larval dispersal with the prevailing coastal current. In Paper III I investigated together with colleagues the genetic population structure of edible crab stock in Swedish waters using microsatellite DNA. In this study we found a a lack of spatial and temporal genetic differentiation between crab stocks in Kattegat, Skagerrak and even up to Ålesund, Norway – a waterborne distance of 1300 km. Local management of the edible crab can be considered and implemented whereby stakeholders take a precautionary approach such as implementing landing size restrictions, not fishing below a certain local biomass or above a defined fishing mortality.

In paper IV we present an estimate of the total abundance of crabs on the Swedish west coast, based on a combination of experimental fisheries to get effective fishing area and catch per unit effort data, and GIS modelling of available crab habitat. In a mark-recapture experiment in the

Koster fiord area we estimated the effective fishing area around crab pots targeting edible crabs i.e. the area from where the crabs are captured if the pot was 100% effective at catching crabs, to 2293 ± 1137 m2 (mean ± 95% confidence interval), corresponding to a circle with a radius of 26.6 ± 6.3 m. In a separate experimental fishery in the Fjällbacka archipelago (35 km south) we estimated catch per unit effort at two depths strata (15-18 m and 25-30m) at 7 locations during two seasons. Using the estimated effective fishing areas around the string we calculated an average density of 0.0038 ± 0.0015 crabs/m2. The area of suitable crab habitat in the Swedish part of the Skagerrak and Kattegat, 10 and 40 meters water depth, and with a bottom consisting of bedrock, stone, gravel or sand, was estimated to 4142 km2. This suitable crab habitat combined with the density estimates from Fjällbacka would indicate that the catchable population of crabs on the Swedish west coast would be approximately 10-22 million (95 % confidence interval) of crabs.

In paper V we assessed stock indicators such as fishing mortality, stock abundance and egg production. The assessments were based on estimations of growth parameters and resampling of parameter values in a length cohort analysis (LCA). The fishing mortality of females was larger than for males both in Kattegat and in Skagerrak. This pattern can be explained by the higher market price for females, so that fishermen choose female dominated grounds and/or land more females. Another possibility is that the catchablity of females in general seems to be higher during the main landing autumn period. The fishing mortality in the investigated area seems to be low. The stock biomass of edible crabs available for the Swedish fishermen in Kattegat and Skagerrak is estimated to 4-8 million edible crab or 1600-2600 tonnes. This stock estimate is based on official data on the Swedish commercial landings and estimated recreational landings, i.e. approx. 400 tonnes in total, and is highly dependent on the total landings and on the input values of growth parameter and natural mortality.

The status of the edible crab stock in the Kattegat and the Skagerrak appears to be good. The fishing mortality is low and no trend (decreasing or increasing) in logbook landing per unit effort (LPUE) can been seen over the last 13 years. Since 2004, using landing and effort data from logbooks for vessels > 10 m, the LPUE is on average around 2.0-2.5 kg/pot.

This thesis provides new and increased knowledge concerning the sexual maturity, migration potential, and genetic population structure of the edible crab in Kattegat and Skagerrak and provides the first estimates on the total stock based on LCA modelling as well as an stock estimate using crab density and suitable crab habitat.

Keywords: Cancer pagurus, Swedish west coast, sexual maturity, migration, population genetics, stock structure, fishing mortality, stock abundance, management

SVENSK POPULÄRVETENSKAPLIG SAMMANFATTNING Krabbtaskan (Cancer pagurus) är ett tiofotat kräftdjur som fiskas kommersiellt i stora delar i dess utbredning i Europa längs nordost Atlantiska kusten. Det största fisket sker på Brittiska öarna. På ett ungefär landas årligen 20 000-25 000 ton i Storbritannien, 10 000 ton på Irland och 6 000 ton i Frankrike. Norge har fyrdubblat sin landning över en tidsperiod på 10 år och landar nu över 8 000 ton. Sverige kan i dessa sammanhang betraktas som ett utvecklingsland med officiella landningar kring 150 ton. Om en skattning av fritidsfisket inkluderas ligger den totala landningen kring 400 ton.

Min forskning har varit fokuserad på förvaltning av krabbtaskan i Västerhavet. Jag har dels studerat om den nuvarande förvaltningsformen (flyktöppningar) är tillräcklig för att säkerställa rekrytering till beståndet dels har jag undersökt en viktig grundegenskap för hållbar förvaltning hos kommersiella bestånd, nämligen dess beståndsstruktur. Med beståndsstruktur menar man att om det finns olika bestånd som är avskilda från varandra, och på vilken geografisk skala som bestånden kan urskiljas eller om det inte finns någon egentlig gruppering. Jag har även gjort en skattning på hur hårt beståndet är fiskat och två av varandra oberoende skattningar av beståndsstorleken samt en genomgång av Fiskeriverkets loggboksdata.

I manuskript I undersökte jag vid vilken storlek krabborna blir könsmogna. För att ta reda på detta studerade jag krabbornas ägg- och spermie produktion, och om honorna hade parat sig genom att se om de hade spermier i förvaringsorganet och om nyömsade honor hade en s.k. kalkplugg i könsöppningarna. Jag mätte även honornas bakkropp som omfångar de yttre befruktade äggen, och hanarnas klor som används vid försvar och vid parning. Resultaten visar att vid en skalbredd om 132 mm har 50 % av honorna äggproduktion (fysiologiskt könsmogna) men parning sker redan i stor utsträckning vid en skalbredd om 107 mm. Hanar är fysiologiskt mogna (50 % av individerna) vid 101 mm alternativt 122 mm beroende på hur konservativt man bedömer en hanes spermieproduktion. Men, det finns tecken på att de honor som verkligen är könsmogna d.v.s. de har yttre befruktade ägg, är ännu större. Äggbärande honor fångas endast i litet antal varför det är svårt att basera en undersökning på denna karaktär. Skalbredden på de äggbärande honor som fångas ligger främst kring 150 mm. För att ge 50 % av honorna en chans att reproducera sig rekommenderar jag ett minimimått på 140 mm. Detta böra gälla både för honor och hanar då små hanar kan ha en sämre förutsättning till parning (konkurrens med stora hanar samt att för parning med stor hona krävs en stor hane). I och med detta bör också storleken på flyktöppningar justeras till 90 mm, från dagens 75 mm i diameter. I manuskript I har jag även studerat hur många befruktade ägg en hona av varierad storlek bär på, och vilket uppgår till 0.5- 2.5 miljoner ägg.

Beslutfattande inom svensk fiskeriförvaltning sker vanligtvis från ett uppifrånperspektiv, en art förvaltas ofta över ett stort geografisk område och tillträdet till resursen är ofta öppen för alla licensierade yrkesfiskare. Ett alternativ till dagens förvaltningssystem kan vara att införa lokal samförvaltning där en grupp fiskare och andra intressenter får fiskerätten inom ett område eller till ett fiske. Nyttjarna får då en ökat ansvarskännande och värnar mer om ”sin” resurs. Men passar en lokal förvaltning alla bestånd, och vad behöver man veta om artens biologi? Det man främst behöver känna till, och det gäller egentligen all förvaltning, är hur beståndet är fördelat i rummet. Består resursen av ett sammanhängande bestånd eller finns det mindre grupperingar som står för sin egen rekrytering och är oberoende av omkringliggande grupper. I manuskript II har jag och kollegor studerat hur krabbor vandrar längs svenska kusten. Detta gjordes genom märk- återfångst experiment dels i slutet på 1960-talet dels i början av 2000-talet. Totalt märktes ca 3700 krabbor respektive 8000 krabbor i dessa experiment. Det vi kunde visa var att honor vandrar betydligt oftare och längre än hanar. Honor vandrade distanser om mer än 100 km, och

även upp till 228 km medan det största avståndet för hanar var 60 km men ofta kortare. De längsta vandringarna om 20 km och uppåt är huvudsakligen mot syd. Hanarna vandrade inte i någon specifik riktning. Honorna vandrade med en högre hastighet under hösten i jämförelse med sommaren men det var inte någon skillnad i vandringsbenägenhet mellan olika storlekar. Orsaken till honors vandring tros vara att de vandrar mot den förhärskande strömriktningen innan larvkläckning för att kompensera att larverna förs med strömmen. I svenska vatten stämmer denna hypotes till viss del men som vi visar i manuskript II så sker en hel del långvandringar mot norr, med strömmen. Med hjälp av genetiska analyser kan man få reda på hur genetiska lika eller olika krabbor är från olika områden. I manuskript III visar vi att det inte finns någon genetisk skillnad mellan krabbor i Kattegat och i Skagerrak, och faktiskt gäller detta hela vägen upp till Ålesund i Norge, ett avstånd på ca 1300 km. Detta beror då antingen på att det finns ett stort genflöde (larvspridning och vandring) mellan krabborna från dessa områden. Det kan också bero på att krabbor från olika områden inte har hunnit att bli olika i sin genetiska sammansättning efter att krabborna återkoloniserat Kattegat och Skagerrak efter den senaste stora inlandsisens reträtt för ca 10 000 år sedan. Baserat på undersökningarna i manuskript III drar jag slutsatsen att krabbor inte har någon genetisk differentiering i Västerhavet och kan betraktas som ett genetiskt bestånd. Detta leder också till man kan förvalta krabban på lokal basis då man inte riskerar att genetisk utarma ett helt bestånd. Man bör dock ha kommunikation mellan samförvaltningsgrupper så att man har en översikt på hela beståndet och naturligtvis inte fiska för hårt inom det lokala förvaltningsområdet.

I manuskript IV har jag och kollegor undersökt över hur stor area som en bur fiskar d.v.s. över hur stort område som en bur täcker för att fånga alla krabborna i buren. Detta gjordes genom att släppa ut märkta krabbor på olika avstånd (10-160 m) i fyra riktningar runt en bur, och se proportionen varifrån de fångade krabborna kom. Den effektiva fiske area skattades till 2293 ± 1137 m2 (±95 % konfidens intervall) vilket kan omräknas till en cirkulär area med radien 26.6 ± 6.3 m. I ett annat fiskeexperiment undersökte vi hur stor fångst per ansträngning som fås vid under olika säsonger, djup och dagar, och med hjälp av den effektiva fiske radien skattade vi tätheten till 0.0038 ±0.0015 krabbor per m2. Den totala area som krabbor i Västerhavet möjligen befinner sig på (10-40 m djup, hårdbotten såsom berg, sten, grus, sand) skattades med hjälp av GIS modellering till 4142 km2. Därmed skattas den totala mängden fångstbar krabba till 10-22 miljoner krabbor.

I manuskript V har jag tillsammans med personal på Fiskeriverket gjort en beståndsuppskattning av krabba i Västerhavet. Vi har använt en metod som kallas längd-cohort analys som bygger på att man har kännedom om längdfördelning i den totala fångsten och antagandet att en minskande mängd av allt större storleksklasser beror på dödlighet. Genom att man vet hur stor del av varje storleksgrupp som blir fiskade och antagande om hur många som dör naturligt (predation, ålderdom) kan man räkna baklänges för att få reda på hur många det måste ha funnits i början av tidsperioden. Sedan summerar man ihop medeltalen för alla längdgrupper och får ett totalt antal som finns i havet, eller en total biomassa då vi vet hur mycket krabbor av olika storlekar väger. För den skattade totala landningen på 401 ton har vi skattat beståndsstorleken till mellan 4-6 miljoner krabbor eller 1600-2600 ton. Den könsmogna andelen honor producerar årligen mellan 5-7x1011 ägg men hur stor del av dessa som överlever och ger rekrytering till beståndet har vi ingen uppfattning om. Med ovan metod kan man också skatta fiskeridödligheten, och vi fann att denna var högre för honor är för hanar. För båda könen är dock dödligheten från fisket låg, om man jämför med andra områden i Europa.

Min avhandling ökar kunskapen om storlek vid könsmognad, äggproduktion, vandringspotential, genetisk beståndsstruktur och mängden av krabba i Västerhavet.

List of papers

This thesis is based on the following papers referred to in the text by their roman numerals. The papers are appended at the end of the thesis.

I. Ungfors, A. 2007. Sexual maturity of the edible crab (Cancer pagurus) in the Skagerrak and Kattegat, based on reproductive and morphometric characters. ICES Journal of Marine Science 64:318-327. II. Ungfors, A., Hallbäck, H. and Nilsson, P.G. 2007. Movement of adult edible crab (Cancer pagurus L.) at the Swedish West Coast by mark-recapture and acoustic tracking. Fisheries Research, 84:345-357. III. Ungfors, A., McKeown, N.J., Shaw, P. and André, C. Lack of spatial genetic variation in the edible crab (Cancer pagurus) in the Kattegat-Skagerrak area. Submitted manuscript. IV. Ungfors, A., Nilsson, P.G. and Sundström, H. Effective fishing area, crab density and stock abundance of the edible crab (Cancer pagurus) in Swedish waters using mark-recapture experiment and GIS modelling. Manuscript. V. Ungfors, A., and Ulmestrand, M. Stock indicators of the edible crab (Cancer pagurus) in the Kattegat and Skagerrak estimated by length cohort analysis and resampling of growth parameters. Manuscript.

Already printed papers are reprinted with kind permission of the copyright holders, Oxford Journals (paper I) and Elsevier (paper II).

A doctoral thesis at a university in Sweden is produced either as a monograph or as a collection of papers. In the latter case, the introductory part (the summary) constitutes the formal thesis, which summarises the accompanying papers. These have already been published or are manuscripts at different stages (in press, accepted, submitted or in preparation).

Contents

INTRODUCING CONTEXT OF THE THESIS...... 11

AIM OF THE THESIS ...... 11 FISHERIES DYNAMICS...... 12 MANAGEMENT...... 14 Regulations...... 14 Management of edible crab stocks ...... 15 LIFE HISTORY OF THE EDIBLE CRAB...... 19

LARVAE AND JUVENILES ...... 19 GROWTH ...... 20 SIZE AT MATURITY AND FECUNDITY – PAPER I ...... 22 Histological examination of gonads...... 24 LONGEVITY AND NATURAL MORTALITY...... 26 STOCK STRUCTURE ...... 26

THE GEOGRAPHIC AREA OF THE THESIS ...... 26 BACKGROUND STOCK STRUCTURE ...... 27 MOVEMENTS – PAPER II ...... 28 POPULATION GENETICS – PAPER III...... 31 SPATIAL AND TEMPORAL VARIATION IN PHENOTYPIC TRAITS ...... 33 STATUS OF THE SWEDISH EDIBLE CRAB STOCK ...... 36

DENSITY ESTIMATIONS – PAPER IV ...... 36 STOCK ASSESSMENT – PAPER V ...... 37 LOGBOOKS ...... 39 CONCLUSIONS ...... 42 SWOT ...... 42 LOCAL MANAGEMENT OF EDIBLE CRAB...... 44 RESEARCH PERSPECTIVE ...... 45 ACKNOWLEDGEMENTS (TACK) ...... 46 REFERENCES...... 48

10 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Introducing context of the thesis

Aim of the thesis With few exceptions marine resources in Europe are today managed either on national or on EU level. The management unit and the biological definition of a stock may not coincide. In the wake of failures in finfish management recent initiatives such as local co-management of fisheries, considering a smaller management area with larger co-operation and responsibility of stakeholders, are under consideration. However, how compatible is this new approach to the biological stock concept?

Within the MISTRA-programme SUCOZOMA (sustainable coastal zone management) different species within the Baltic Sea and on the Swedish west coast have been investigated for the purpose of local management. In this thesis I have investigated life history traits such as migration potential and genetic variation of edible crab Cancer pagurus in Kattegat and Skagerrak (ICES area IIIa) to assess connectivity and stock structure. These are important input data for evaluating which geographic levels are suited for sustainable management. The edible crab was chosen because of its potential for an increased interest from fishermen and consequential increase in exploitation and need of management recommendations, and for being a marine crustacean species with a different life history, inhabiting a more "open" environment compared to Baltic fish species.

The thesis has also evaluated if the present management strategy using an escape gap of 75 mm diameter in fishing gears acts to protect the stock from fishing individuals before reaching sexual maturity. Today, a minimum landing size is not implemented in the area. This technical regulation is important disregarding the geographical scale of management unit.

Fishery biological characters such as size (carapace width) and sex of the captures and the catch per unit effort (CPUE) are important for assessment approaches, and have been sampled in commercial captures of the edible crab in the fishery area Kattegat and Skagerrak. Based on these data, stock assessment has been carried out with estimates of stock parameters as fishing mortality and abundance. Also, we have investigated how different input parameters impact these. In addition to this modelling approach to estimate abundance, a method using our experimental estimate of density (independent estimate of gear effective fishing area and CPUE) and extrapolation over suitable crab area using GIS, is presented.

The topics in my thesis were chosen in the spirit of local management to define stock structure (paper II and III), and by my identification of maturity analyses (paper I) and abundance estimates (paper IV and V) as being high-priority research areas for sustainable recruitment of the stock and a sustainable future fishery. In the coming chapters I will present my results in a fishery biology context. In this chapter I start by giving a general introduction of the fisheries dynamics i.e. what is changing over time in a new fishery (effort, stock abundance, gears, skills, area covered), I then give a an overview of management regulations and a detailed picture of the fisheries and management of edible crab across its geographic distribution. In the chapter about “Life history of the edible crab”, I present biological traits of importance to management which I have been working with. In the chapter on “Stock structure” my methods and findings on this subject are summarized (paper II and III), and in the chapter on “Stock status” I summarize my (together with colleagues’) assessments (paper IV and V) and an analysis of the logbooks (Swedish Board of Fisheries). In the final chapter “Conclusions” I have listed the presence and

11 11 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) absence of essential knowledge, and the pros and cons (SWOT) of the edible crab biology for sound fisheries. I also give an overall conclusion on the local management issue. In addition I briefly present my perspective on a continued edible crab research.

Fisheries dynamics Nellerman et al. (2008) have recently summarised the impact on the oceans by man. All oceans show traces of impact or even large environmental changes due to a wide range of human activities such as destructive fishing methods, pollution and invasion of foreign species. Reducing the overcapacity is top priority in the EU common fishery policy (CFP). On the Swedish level there have been an unusually large amount of fishery related issues in the media: a debated and prized book trying to analyse the causes and the different views of depleted fish stocks (Lövin 2007), newspaper articles and television panel debates have succeeded, mostly considering fin fishes as the cod, Gadus morhua. However, in contrast to the finfish fishery, an optimistic view on crustacean fisheries is often expressed. Crustacean fisheries worldwide are becoming more important and in 2005 accounted for 6 % of the world capture production by weight but 26 % by trade value (FAO). Many crustacean fisheries are artisanal, but their importance from a socio-economic perspective should not be neglected.

The dynamics of a fishery over time can broadly be described as going from a pre-developmental phase where the news of a potential profitable stock is spreading, to a growth phase where the fishing fleet and effort is rapidly building up the capacity, and then reaching the fully exploited stage (Hilborn&Walters 1992). At full exploitation, fishing success has normally declined as more fishermen compete for the resource, and this decline in fishing success, or management, may set a further limit on fishing pressure. However, overexploitation and collapse may follow, especially if governmental subsidies are offered, which decrease the exploitation costs for fishermen. In an unregulated, open access fishery, effort might expand to the level at which total revenue equals total cost, called the bionomic equilibrium (Clark 1985). At this stage the growth of the fleet size comes to an end. Low costs make it possible to keep a fishery at low revenue, e.g. at biologically overfished stocks, and the more valuable a fishery (high price/cost), the more intensively it will exploited. But from the fishermen’s point of view the optimum effort level occurs where the difference between revenues and costs is maximised, often called the maximum economic yield (MEY). However, to stabilise the fishing effort at MEY requires management restrictions of the fishing effort, as an open access otherwise may lead to bionomic equilibrium where revenue equals cost.

Many times the biological knowledge about stocks for which commercial exploitation has only recently started is low, and the reactions from authorities often come after indications of overexploitation. Life history traits such as longevity of the species, age at first spawning and migration behaviour can give an early indication of the risk of collapse of the stock (Perry et al. 1999). In the early stage, the distribution of a fishery is often coastal with relatively short distances to harbour. The fishery may then evolve to occupy a wider area off-shore, while the fishing fleet and capacity is increasing. Larger fishing vessels and/or more efficient engines are often the basis for a wider fishing area. Catch per unit effort is decreasing or taking downward steps during exploitation but records of increased catches especially for schooling fish before a collapse are well-known, often claimed to be caused by a narrower distribution of the remaining fish. The effort in a fishery is not homogenous, neither in time nor in space. The fishing area covered by the gears is not homogenous in terms of available resource as the substrate and species composition varies. Local knowledge of fishermen includes empirical experience of bottom substrate, and knowledge of “good and bad” fishing grounds. The definition of an area as

12 12 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) good or bad may differ with season and year. In addition, the fishing gears are becoming more efficient, often through a tendency towards larger gear. However, in a crustacean pot fishery many smaller pots can be advantageous. The invention of the parlour pot, with an extra room or safety chamber, resulted in increased catch per pot by increasing the days at sea. Thus by decreasing the number of escapes and increasing the attraction period, it provided to be profitable to lift the pots more seldom. This gave the possibility for alternate use of a large number of strings with pots, leading to an increase in catch per pot and extra revenue after the initial cost for a larger amount of gear. Comparison of the catch per unit effort in a fishery over time needs to consider these changes in e.g. effort and allocation of the fishery. In other words, the landing data need to be standardised. Standardisation can be reached by different means: use of time-series of research surveys with same gear and effort, research fishing on different habitats to be able to account for different capture potential, time overlapping use of different gear, or by statistical methods such as generalised linear models to identify the most important factors and the impact on capture of those. Therefore, knowledge of the fishermen’s behaviour such as increased skills and movements between fishing grounds, should be considered to the same extent as biological studies in fisheries science (Hilborn&Walters 1992).

Crustacean fisheries have shown the different stages from unexploited to a depleted stage often accompanied with an increase in effort capacity. The fishery for Red king crab (RKC) Paralithodes camtschaticus in the Bering Sea around Alaska increased heavily in landings in the 1970´s but peaked in 1980 and thereafter more or less collapsed. A combination of high exploitation rate and increased natural mortality in the late 70´s (Zheng et al. 1995) caused the collapse in the RKC fishery. This fishery has still a high economic value, but comparing the 59000 tonnes of Bering Sea landings in 1980 with 8200 tonnes in 2005 shows the extent of the stock decrease. An up and down crab fishery in the Bering Sea have also been seen for the snow crabs Chionoecetes opilio which peaked in 1991 with 149 000 tonnes, declined thereafter and are now around 10 000 tonnes. In addition to regulations such as minimum landing size, male only fishery, pot limits and seasonal closures, Individual Fishing Quotas (IFQ) have recently been introduced in these fisheries. A RKC fishery is now established in the Norwegian Northern fiords bordering Russia. The crabs have dispersed into the northern part of Norway from the Murmansk area, Russia, to which it was deliberately introduced in the 60´s (Orlov&Ivanov 1978). Red king crabs were observed occasionally in the 70´s in Norwegian waters and a research fishery started in 1992-93 with few vessels with many restrictions (individual quota, specific season, minimum landing size, male landing) and mandatory co-operation with the researchers. The RKC have caused problems as by-catch in the demersal trawl and net fisheries for codfishes. Jointed stock assessments were performed by Russia and Norway during some years but since 2002 Norway assess their stock and set their Total Allowable Catch (TAC), based on annual research surveys. TAC in 2007 was 300 000 crabs, for males only > 137 mm carapace length. The RKC stock and fishery might possibly have reached highest levels as authorities will try to restrict the crab´s further southward distribution by a open fishing west of longitude 26°E (Anon 2007b).

The blue crab (Callinectes sapidus) is the base for the most important commercial fishery in the Chesapeake Bay, USA. Commercial landings in 1993 have exceeded 45000 tonnes with more recent average landings reaching approximately 36000 tonnes. The total impact of the blue crab fishery to the Chesapeake region exceeds $200 million annually. In 1998 the Bi-state Blue crab Advisory group stated that the crab population was not in a healthy condition, based on findings on decreasing abundance of all age groups, low spawning stock, decrease in average size in combination with high fishing mortality and effort. The new management framework identified biomass- and exploitation reference points. Rigorous assessments (Miller et al. 2005) now

13 13 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) indicate that the stock is not experiencing overfishing as it did for a period in the late 1990’s and early 2000’s. However, the abundance is still not at former levels.

In addition to changes in the resource abundance caused by fishery, natural variation in recruitment and mortality also has an impact on the abundance. Natural variation has been studied using deposition of fish scales in anoxic sediment for e.g. herring and anchovy (Patterson et al. 2005). Caddy and Gulland (1983) classified exploited stocks into four groups; steady state, cyclical, irregular and spasmodic, based on abundance pattern. The cause behind these patterns may be a combination of natural and fishing mortality.

Management The exploitation of marine resources has resulted in a large number of books and papers filled with theories and models trying to understand the nature of the resource and the exploitation effect (Beverton&Holt 1957; Ricker 1975; May 1984; Clark 1985). Models are simplifications of the real world and the major task is to determine how to simplify without losing the ability to understand the reality and inform management of options. Parameters of interest such as fishing mortality and stock size can be estimated, and are used to provide management advice. A major failure of conventional fisheries advice is that it generally does not explicitly incorporate important sources of uncertainty. Stock or risk assessment aims primarily at evaluating the consequences of various harvest strategies for future trends in yields, biomass, and dangers to the stock (Hilborn&Walters 1992). Another key role of stock assessment is to identify if catch and effort statistics give a false picture of the population dynamics, and if a more extensive sampling programme is necessary and worthwhile. Data are collected from e.g. logbooks, commercial or recreational fishermen’s own notes and from research vessel. Incentives is another management tool used, such as allowed increased catches or access to other periods and areas for fishermen spending part of their time “fishing for information”. In assessment models using sex-and size specific parameters of the catch, catch data collected by co-operative fishermen is essential (in addition to research surveys) as logbooks are often not that detailed. Risk management on the other hand, involves finding and implementing management policies, strategies, and tactics that reduce the risk of over-exploiting the stocks (Hilborn et al. 2001).

Different levels of stock assessment occur: from descriptive statistics on catch, to some findings of population structure and abundance indices, and to fully analytical risk assessments attempting to understand the stock and fishery dynamics, and estimating population parameters. A less informative assessment of a stock leads to a reactive management i.e. reaction from authorities when CPUE is decreasing or a fishery becomes unattractive for fishermen due to low landings. However, a more comprehensive assessment provides the means for an optimal management (Smith&Addison 2003). As a response to declining annual catch rates of Tasmanian rock lobster Jasus edwardsii from 1.6 to 0.9 kg/pot between the years 1980-1995, assessment and management have improved (Punt&Kennedy 1997). Stock assessment are performed for eight regions and the stocks are managed by Individual Transferable Quotas (ITQ), limited entry, gear restrictions, closed seasons, MLS, bans on working gear at night and on taking berried females. Recreational fishers are allowed to use a single pot. Adaptive management, which is a combination of quantitative modelling and empirical management “experimentation”, can be seen as a mixture of reactive and optimal management.

Regulations Management of marine stocks involves control of exploitation by limitations in effort (e.g. gear specifications, days of fishing per boat and year, engine capacity, seasonal closures) or

14 14 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) limitations in landings (e.g. total allowable catch TAC, individual transferable quota ITQ, maximum landings per week or season). Regulations can also be based on a minimum or maximum landing size (MLS), sometimes in combination with a selective gear mainly capturing individuals over respectively below a certain MLS. Limitation of either nature is based on knowledge or estimations of how the stock responds to different fishing mortality (F), and reliable processes to translate the fishing mortality into practical legislation expressed as effort or yield. To avoid growth overfishing i.e. fishing too small juvenile individuals the fishing mortality (FMSY) where the yield of the stock is maximised (MSY), is a target to be obtained, or rather a limit not to exceed. Avoidance of recruitment overfishing, i.e. fishing too heavy on mature adult individuals which give rise to the next generation, is harder to avoid as the relationship of stock and recruitment is complex. In both categories, for avoidance of overfishing, a precautionary approach using precautionary targets (amber warning light) and limits (red light) are used as reference points e.g. for the fishing mortality (Fpa, Flim) or biomass of spawning stock (Bpa, Blim).

Use of property rights in fisheries management is widely discussed (Shotton 2002; Brady&Waldo 2008). A property right can be in the form of an ITQ (New Zealand), an assigned number of Days at Sea (Faeroe Islands) or exclusive admission to a fishing area (local management). The advantage of establishing property rights is that the users may take a larger responsibility for the future of the resource, avoiding the “tragedy of the commons”. Implementing transferable rights as ITQ can however lead to fewer and larger vessels if no restrictions are defined. For the Irish crustacean fishermen, life-time licenses with a chance of transferability to a family member, e.g. on retirement, guided by a public decision-making committee are recommended so as the licences would not become commodities (Bradshaw&Tully 2004). In Sweden, the national authorities are presently investigating a possible introduction of ITQs for the pelagic fisheries. In addition, license requirements have been introduced for e.g. the shrimp fishery and the Nephrops creel fishery in order to safeguard the resources and enable economic viability for the fishermen historically involved in the fisheries concerned.

Marine protected areas (MPA) can be used to protect a habitat as well as the exploited fish and crustacean resources within. The degree of restriction within the area varies from being totally protected from any kind of use, to zone (Hiddink et al. 2006) where specific fisheries are banned and others allowed. The process for implementing MPAs has been diverse, ranging from being a top-down project (governmental) to a local initiative. The effect of an MPA, especially in temperate regions, on the resources concerned are widely debated, hence several scientific programmes are looking into this (Protect at www.mpa-eu.net/; EmpaFish at www.um.es/empafish/).

Management of edible crab stocks Crab species have become some of the most valuable fisheries within the ICES North Atlantic area. As fishing effort has been increasing in recent years there is need for proper assessment and management advice (ICES 2007). The ICES working group on the Biology and Life history of Crabs (WGCRAB) has participants from most countries with edible crab fisheries, and collects data on landings, discards, effort and CPUE as well as recommending standardised methods for sampling of these data at regular workshops. The focus for the WGCRAB is moving towards defining appropriate management units and evaluating potential assessment methods based on data availability.

The distribution of the edible crab is the European Atlantic Coast from Tromsø, Norway to Portugal (Christiansen 1969 and pers. comm. Astrid Woll). In most parts of the edible crab

15 15 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) distribution area a minimum landing size is implemented, either of national (UK, Addison&Bennett 1992; Norway, J-102-2004) or international status (Anon., Council regulation (EC) no. 850/98). However, the crab fishery in the Swedish territory and economic zone of Skagerrak and Kattegat is not regulated by a MLS but by mandatory 75 mm escape gaps in crab pots (figure 1) and in fyke-nets (Council regulation (EC) no. 850/98; FIFS 2004:36). The Swedish escape gaps allow crabs of carapace width (CW) below 110-115 mm to escape (Dybern 1983). In the northern part of Skagerrak, from the Swedish border to the Norwegian south west coast (Rogaland) commercial landing of crabs < 110 mm is prohibited (Anon 2004b).

Figure 1. Escape gap of 75 mm diameter mandatory in edible crab pots in Sweden. Photo: Anette Ungfors.

Below is a summary of landings, available data, stock status and management regulations per country, mainly based on ICES WGCRAB report from 2007 (ICES 2007), if no other reference.

United Kingdom – Landings in England and Wales have increased by an average of 400 tonnes per year since the early 1980s (ICES 2005). The majority of the landings originate from ICES sub-areas VIID and E (Western English Channel: approx. 5000 tonnes) and from IVB and C (North Sea: approx. 4500 tonnes) (ICES 2005). Despite the large landings in England and Wales the data reporting system of the fisheries is limited especially for the effort. However, the system has improved from consisting of the official Fishing Activity Database since 1983 with underestimations of landings and poor effort data, added with EU log-books for vessels > 10 m in 2000 but which were limited in the first years by bias in effort recordings, and further improved in 2006 with mandatory log-books for vessel < 10 m. The 2006 landing in all stock management units increased sharply as a result of the mandatory logbooks of smaller vessel. Six stock management units (SMU) have recently been implemented: Western Central North Sea, Southern North Sea, Eastern Channel, Western Channel, Celtic Sea and Irish Sea. The fishery effort peaks during the summer months, which reflects the dependency on weather conditions whereas the landings peak in autumn-early winter. The fisheries are regulated by minimum landing sizes specified for different areas (115 mm CW in Norfolk area, 160 mm for males and 140 mm for females in Western Channel and south eastern parts of Celtic Sea, and 140 mm CW for rest of the area for males and females). Landings of soft-shelled and ovigerous crabs are prohibited. Landings in Scotland fluctuate between 6600-9400 tonnes since 2000. The main fisheries are around the Shetlands Isles and Orkney Islands, and off the northwest and west coasts. The Shetland fisheries (approx. 300 tonnes) are managed locally within 6 nautical miles. All vessels must obtain a license from the Shetland Shellfish Management organisation, and the fishermen are required to fill in logbooks for 5-mile squares. In conclusion, landings in the whole UK is around 20 000-25 000 tonnes per annum.

Ireland –The crab landings have increased by approx. 650 tonnes annually from 1990 to 2004 from less than 4000 tonnes to over 13 000 tonnes. During this period the annual effort for the area

16 16 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) has increased from about 28000 to 1 396 800 pot hauls. Excluding the exceptional 2004 landing, the landings seem to be stabilised around 10 000 tonnes since 2001. Detailed capture records exist for the offshore segment consisting of 3-5 index vessels from 1990 and onwards. In addition of precise landing and effort the position is given which mean that changes in catch rate can be associated with moves in the geographic location of fishing, rather than changes in stock abundance. The short but intensive periods in a given area have also been used in stock assessments by depletion methods (ICES 2003). In the offshore area the LPUE has decreased stepwise from 2.6-2.8 kg/pot in 1990-1992 to 1.3 kg/pot in 2006. This decrease is robust to changes between years in seasonal and spatial allocation of the fishery (Bell et al. 2005) using GLM. The inshore data are not of the same accuracy as the offshore data but LPUE have been falling to a similar extent. Fahy (2002) points at an extended under-estimation in official statistics of the landings in the south-eastern Ireland. The MLS in Ireland is 130 mm CW (ICES 2004).

France –The annual landings have decreased over the period since 1984, from 7292 to 5423 tonnes, coinciding with a decrease in number of coastal potters. Potters provide 75 % of the landings and the rest is taken by gillnets and trawlers. The offshore potters land 40% of the total landings. Since 1985 there exists a relatively good database of fishing activity of this limited offshore fleet consisting of 15-25 vessels. Over this period the number of offshore potters decreased but the number of pots/vessel increased from 700 to 1000. The CPUE shows no long- term trend for any area. The French edible crab fishery is regulated by licenses and pot limitations (maximum 250 pots per fisherman and 1000 pots per boat), which have been in use for more than 10 years. Parlour pots are banned.

Norway – There has been a fourfold increase in landings of the edible crab during the last 10 years, from 2000 to over 8000 tonnes in 2007, which is a result of directed effort from the industry to exploit and process this resource but also from an increase in the distribution and exploitation of the crab towards northern areas. Research projects financed by the government, community and industry are focusing on market issues such as quality grading by a developed light penetrating device, quality improvement by artificial feeding and live-storage (Woll&Berge 2007), on resource investigations (Woll et al. 2006) and how to use by-product from processing (Østvik et al. 2006). From 2001, on research basis and from 2004 and onwards on permanent basis, contracted fishermen have filled out detailed capture protocols for 4 standard pots during a 10-week period. The pots must be deployed twice a week, and are spread among the rest of the gear. The fisheries are divided into 5 districts and from where the main landings are taken between 62° to 67° (area 06 and 07; county Møre og Romsdal, S and N Trondelag and Helgeland). No obvious trend in LPUE or DPUE (discards) has been found for any of the southern areas but higher LPUE for the most northern area (area 00 Lofoten and 05 Vesterålen). The fishery is regulated by minimum landings size of 130 mm CW north of 60° and by 110 mm south of this latitude. Landings of soft-shelled and ovigerous individuals are banned. Landings in Skagerrak are under-estimated, as fishermen are not obliged to report the landings to the fish sale organisation.

Sweden - The edible crab in Sweden is distributed in the Kattegat and the Skagerrak, and is commercially fished in these areas. The fishery of edible crab in Sweden is small-scale. Recordings of annual landings based on the trade by first-hand dealers exist from 1914 onwards (figure 2) and vary between 50-233 tonnes. The high reported landing in 1994 is probably due to a new license system: for a renewed license the fishermen had to report landings. Many types of gear capture the edible crab but gears targeting crab and lobster are most important. Gear such as pots, gillnets or fyke-nets targeting crabs or lobster took 82% of the landings in 2006.

17 17 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Figure 2. Swedish edible crab landings in 1914-2007 based on first-hand sales. Source: the National Statistics Office of Sweden.

Records of annual landings, based on data from logbooks and first-hand dealers over the last twelve years from 1994-2007 (figure 3), show some cyclic variation between years. Reports from first-hand dealers (white triangles) are on average 33 tonnes lower than logbook data targeting crab or lobster (dotted line white squares), and total landings (thick line filled diamonds) on average 21 tonnes higher than those based solely on logbook data from vessels targeting crab and lobster. The first-hand value of the 134 tonnes landed in 2006 was 280,000. The fishery is allowed all year around but most professional crab fishermen fish during July-November. However, a large unreported amount is taken by recreational fishermen and tourists in summer months. A recent report on the Swedish recreational fisheries has estimated the crab fishery to 269 tonnes (Anon 2007a). Both sexes are harvested, but as the price for females are higher than for males, fishermen tend to choose areas where females dominate (higher female frequency in captures, Ungfors pers. observations). There are few regulations of the Swedish crab fishery. Pots deployed shallower than 30 m must have one, and crab fyke-nets two, circular escape gaps with a diameter of 75 mm (FIFS 2004:36, Anon 2004a). Recreational fishermen are allowed to use six pots, 180 metres of net or six fyke-nets. No gear number restriction exists for commercial fishermen except a maximum of 600 fyke-nets. The European Union has declared a minimum landing size of 130 mm CW but excluded the Kattegat and Skagerrak (Council regulation (EC) no. 850/98).

Figure 3. Swedish edible crab landings in 1994-2007, based on logbook data from the Swedish Board of Fisheries and trade statistics from The National Statistics Office of Sweden.

18 18 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Life history of the edible crab

Bennett (1995) reviews factors in the life history of the edible crab that influence modelling and management. He focuses on the 1) reproductive cycle including findings on maturity and the larvae and the juvenile stage, 2) growth where he discusses sex-specific and regional moult increment (MI) and frequency, 3) movements, 4) catchability changes based on LPUE over the year, 5) population structure mainly indicated by size frequency and 6) stock density in the light of productivity (growth differences), larval occurrence and water currents and adult movements. Below I present my analysis as well as literature data of life history traits that Bennett (1995) identified to be important, and which I also have prioritized. However, I have worked with these traits to a varying degree: most effort has been put into the reproductive trait sexual maturity (paper I) whereas the effort put into other traits e.g. the larvae dispersal simulation is lower but presented as it is an explaining factor for genetic population structure (paper III). Earlier unpublished Swedish data on growth have been analysed in stock assessment paper V. My findings on migration are presented together with the genetic population structure in a chapter of its own (Stock structure). Information on catchability is given in the chapter Stock assessment (paper IV). Literature findings on the longevity, and own calculations, is presented as this is an important factor in life history, which can indicate the vulnerability of the stock to fishery- induced mortality (Perry et al. 1999). Stock assessment often uses estimates on natural mortality, and in paper V I have, together with a colleague, estimated the natural mortality by general life history based models and presented below.

Larvae and juveniles The egg development takes about seven to eight months, and during this period the female lies in the sand, partly buried (Edwards 1979; Howard 1982; Woll 2003). The development of eggs and larvae is temperature-dependent, and the critical minimum temperature is 8-9°C (Lindley 1987). The hatching starts at different times during the year for different regions, and closely follows the pattern of seabed warming above this level. Thorson (1946) found edible crab larvae in the Kattegat during April to October but in general the eggs hatch during summer months June to September (Lindley et al. 1993). During the larval development the planktotrophic, pelagic larvae go through seven development stages; one proto-zoea, five zoeal and finally the megalopa settling stage (Lebour 1927; Ingle 1981). The larval period is a dispersal phase, but different opinions exists about the length of the developmental period; lasting for about four weeks (Edwards 1979), approximately 40 days (Eaton 2005), 60 days as used in a dispersal simulation (Thompson et al. 1995) or even up to 51-78 days including zoea stage IV for laboratory reared crabs in temperatures of 15-20°C (Nichols et al. 1982). The developmental period in 10°C are considerably longer, in total it may take 144 days before reaching zoea stage V (Nichols et al. 1982). Particularly the late zoea stages perform diurnal vertical migration as these are found at deeper depths during daytime compared to dusk and dawn (Irish studies, ICES 2003) which is also found for other Cancer species (Park&Shirley 2005).

Simulation of larval dispersal from a release position near Grove Bank in the Kattegat showed an average dispersal distance of 63 km towards northeast (figure 4) (Jonsson and Ungfors, unpublished). The simulation of larval trajectories was done using the Lagrangian tracking software TRACMAS (Döös et al. 2004) using current velocity fields for the years 1980-2005 modeled with the Rossby regional ocean-atmosphere model (RCAO, Döscher et al. 2002). Dispersal distribution is only based on trajectories ending in areas shallower than 12 metres.

19 19 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Simulated larvae were allowed to disperse for 21 days in April-May, at a constant depth of 0.5-3 m. Of 120 000 released larvae 16.7 % settled within grids shallower than 12 m. Studies of larval distribution have been undertaken around UK and Ireland (Nichols et al. 1982; Lindley et al. 1993; Thompson et al. 1995; Eaton et al. 2003; ICES 2003). Recently, edible crab larvae have been captured in light attracting traps in Skagerrak (pers. comm. Vidar Öresland, IMR, Sweden), which is promising for the future research on the ecology of crab larvae.

Figure 4. Distribution of settled larvae in a simulation of larval dispersal for 21 days from a release point close to Grove Bank in Kattegat, based on current velocity fields from the RCAO model. Only trajectories ending in areas with a depth shallower than 12 metres were used. The mean dispersed distance is 63 km, and the main direction towards NE, to the Swedish coast. Darker colour means higher density of settled larvae. Simulation made by Jonsson, P and Ungfors, A. (unpublished).

Knowledge of the habitat or depth prevalence of Swedish edible crab juveniles is poor but there are occasional observations of juveniles in shallow coastal areas. Four juveniles of carapace width 15-61 mm were caught by bottom-trawl in November 2007 at 6-13 m depth among the brown algae Laminaria digitata and red algae Delesseria sanguinea, Furcellaria lumbricalis Phycodrys rubens and Corallina officinalis (pers. comm. Anneli Lindgren, TMBL). Monthly dive collections of Laminaria hyperborea hapterons (holdfasts) in 1991/1992 at an exposed area in the archipelago in the Norwegian Sea, showed an occurrence of 40 % of crabs in the range of 8-73 mm CW, under the investigated 400 hapterons (Eriksen&Moen 1993). Robinson and Tully (2000) state that shallow water (8-10 m) cobble habitats represent a major source of recruitment to offshore fisheries. In these cobble habitats the authors showed settlement of edible crab 2.5 mm in CW in July to September, but larger sized specimen up to 8.8 mm CW were present in the monthly suction samples taken over one year. In the investigated habitat, the algal cover of Laminaria species varied between 50-70%. In conclusion, further studies of juvenile crab occurrence or abundance in Swedish waters should focus on shallow algal habitat, particular covered by Laminaria species.

Growth The moulting process determines growth in crustaceans, and the growth rate depends on the moult increment (MI, increase in size per moult) and the frequency of the moults. Data on growth increment from Swedish edible crab are based on recaptured moulted individuals in a tagging experiment (Hallbäck, unpublished) and on moults in pots (own measurements) (figure 5). The absolute increment of carapace width (mm) increases with crab size as presented in figure 5, up to sizes around maturity. The decrease in proportional moult (increment to pre-moult carapace width) are shown for females in figure 6 (right graph).

20 20 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Figure 5. Moult increment for females and males. For females, and possibly also for males, the increment seem to decrease (lesser proportional increment) around 100-125 mm CW. The increment is around 25 mm per moult for sizes >110 mm. Data come from recaptures in tagging experiment (Paper II, 1968-73 experiment, increment not presented in the paper) and my observations on moults in pots.

The inter-moult period i.e. the period between moults, which set the frames for moult frequency, is more difficult to estimate. Estimation can be based on intensive mark-recapture studies, observations on moulted proportion per size, observations of laboratory reared juvenile individuals or size frequency data. Estimates on the inter-moult period by isotopes 228Th/228Ra in the pre-moulted carapace (Latrouite et al. 1991; Verdoit et al. 1999) have also been tried. Edwards (1979, and references within) summarise moult frequency based on field and laboratory studies as: following 3-4 moults during the first year a CW of 25-30 mm are reached, during the second year and 2-3 moults 50 mm CW are reached. In the third year the crab may reach 70 mm but further two years are necessary to reach 115 mm. Moult frequency decrease around maturity, possibly more frequently for females than for males. Females may moult every second year to allow sufficient condition and energy demands for gonad development and growth.

In paper V we also plotted a discrete growth curve, for a comparison to the continuous growth based on our estimated von Bertalanffy growth parameters. In this discrete growth curve carapace width is plotted against age (figure 6) based on the findings on moult increment per pre-moult CW, and moult per year discussed above. From the MI data we assumed a 25 % increment increase up to approx. 100 mm CW, thereafter 20 % up to 140 mm, 15 % from 162 mm and 10 % at ca. 180 and 200 mm. From a carapace width of 140 mm (5.5 years old) we onwards assumed a moult every second year. Figure 6 also illustrates continuous Bertalanffy growth curve with L 217 and K 0.160 given, which approximately follow the discrete growth curve.

21 21 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Figure 6. Left graph show female discrete growth curve based on findings of the moult increment (MI) with size for Skagerrak and Kattegat (seen in right graph), and of the estimate of moult interval from Edwards (1979). Right graph show the proportional change (%) in increment to pre-moult CW for females (same data as in figure 6a). MI data originates from tagging experiment in 1968-73 (Hallbäck unpublished) and from my moult observations in commercial pots. Dashed line show the Bertalanffy growth curve for L 217 and K 0.160 (Paper V).

Growth rates have been estimated for the Dungeness crab Cancer magister from size frequency data: 6-9 moults during the first year after settlement, another 2-5 moults during the second year and 1-2 moults during the third year (Wainwright&Armstrong 1993). Tagging of C. magister indicates that older ages moult annually. The probability for annual moult is near one for recently matured females but this probability sharply decreases above 135 mm CW, and approach zero at 155 mm CW (Hankin et al. 1989). This low probability for annual moults occurs at similar sizes for males (Wainwright&Armstrong 1993). Growth of C. magister also shows a marked decrease in moult increment at female maturity size and a less distinct change for males (Wainwright&Armstrong 1993).

Size at maturity and Fecundity – Paper I The reproduction cycle of crustaceans is fairly complex. Copulation of the edible crab occurs when the female recently has moulted, as her shell has to be soft for successful mating. Males and females are attracted to each other before the female casts her shell, probably controlled by a chemical substance similar to a pheromone (Edwards 1966). The male is close to the female during her moult (ecdysis phase) and may even assist the female to escape from the old shell. As the moult is completed the male will gently turn her onto her back and copulation takes place as his spermatophores are transferred to both of the spermathecas of the female, located in her oviducts (Edwards 1966).

After copulation a sperm plug may be produced in each genital opening of the female, seen as white structures visible with the naked eye. The main purpose of the sperm plugs is presumed to be to prevent sperm loss and entry of seawater after copulation, and/or to prevent other males from copulating with the female (Edwards 1979). Fertilisation of the oocytes occurs at the time of spawning, when the mature oocytes are passing the spermathecas (Charniaux-Cotton&Payen 1988). Sperm from a single copulation may fertilise oocytes in several consecutive spawnings (Edward 1979). For the spawn to succeed properly, the female needs a soft bottom substrate while spawning where the eggs are able to adhere to each other and attach to her pleopodal setae. Probably, females do not spawn every year (Swiney et al. 2003).

22 22 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Size at onset of sexual maturity (SOM) needs to be considered in the implementing process of MLS, and signs of mating activities, gonad development or allometric changes in growth of body parts in relation to body size have been used to discriminate between juveniles and adults in Cancridae (Weymouth&MacKay 1936; Edwards 1979; Brown&Bennett 1980; Campbell&Eagles 1983; Orensanz&Gallucci 1988; Orensanz et al. 1995; Hankin et al. 1997; Pinho et al. 2001; Tallack 2002b).

In my study of sexual maturity (paper I), females were defined as mature if the ovary was in a developing or mature stage during the autumn season, or if there were indications of mating activities (presence of sperm in spermatheca or sperm plug of early post-moulted females). For males, two alternative scenarios for the gonad classification were used: gonads classified as developing were defined either as immature (scenario 1) or as mature (scenario 2) as there were definition difficulties with this stage. Morphometric analyses of female abdomen width (AW) and male chela were also used to define SOM. The proportion of mature females based on the reproductive characters, ovary development, spermatheca and sperm plug increased with CW. The CW50, the carapace width where the proportion of maturity is 50%, is 132, 107 and 118 mm, for each character respectively (figure 7). CW50 based on abdomen width is 104 mm, with indications of a change in growth pattern at 95-104 and 125-139 mm CW. The proportion of mature males increases with CW, and the CW50 is 117 mm if the developing gonad is considered immature (scenario 1) and 101 mm if considered mature (scenario 2). CW50 based on chela morphometrics is 122 mm.

Figure 7. Size at maturity ogives (proportion of mature at different carapace widths) for female edible crab in the Kattegat and the Skagerrak (Paper I).

Size at sexual maturity of female edible crabs in Skagerrak and Kattegat is concordant with results from maturity studies in other European areas. A report from the ICES study group on the crab biology and life history points at 130 mm CW as the size of maturity for female edible crab in the North Sea (ICES 2003). Findings on size at sexual maturity (CW50) based on gonad development from different regions are given in table 1. CW50 of females based on gonad development is around 130 mm (as I found for Kattegat and Skagerrak) in Ireland and Shetland whereas smaller maturity size is estimated for e.g. UK and Norway. However, the size distribution of ovigerous females (Hallbäck, H unpublished data, inter-quartiles q25=142, q50=152, q75162 mm, min=109 mm) in Skagerrak and Kattegat, and other European areas (Pearson 1908; Brown&Bennett 1980; Woll 2003), indicate that most females do not spawn until yet another moult. The smallest observed ovigerous female on the English East Coast is 129 mm

23 23 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

CW, but out of 200 the main part of ovigerous females was larger than 152 mm (Edwards 1979). It seems that copulation is established at around 110 mm CW, physiological maturation one moult later (at around 130 mm CW), but that fertilisation needs yet another moult, and occurs around 150 mm. This means that physiologically mature females are vulnerable to the fishery another 1-2 years before becoming functional mature.

To avoid recruitment overfishing, a minimum landings size needs to take into account that we do not have enough data on the size frequency and CW50 of ovigerous functional mature females. Therefore, a precautionary approach setting the MLS above the CW50 of gonad physiological maturity indices, is recommended. Males are functionally mature at smaller sizes but possible limitations for these small males to copulate successfully with larger females may occur why the same carapace width for both sexes can be used. This is most practical when escape gap on the pots should be optimized for the MLS.

Table 1. Size at Maturity – CW50 in different areas within the edible crab distribution. Area Males Females Comment Reference UK Vas deferens/Ovary (Lawler&Addison North Sea 88.9 108.5 2005) Western Channel 94.9 113.7 Eastern Channel 104.9 125.9 Shetland 110-114 130-134 Vas deferens/ Ovary (Tallack 2002a) Ireland Vas deferens/Ovary (ICES 2004) North 112.5 132.6 SW 109.7 138.4 SE 116.8 135.7 Ireland, SW 110 127-139 Vas deferens/Ovary (Edwards 1979) Norway 113.9-117.8 Ovary (macroscopic) (Woll&Emblem 111.8 Ovary (microscopic) 2005) France, Bay of 102 111 Vas deferens ovary/ (Le Foll 1986) Biscay (microscopic)

Fecundity analysis was performed for 39 females sampled in Kattegat and Skagerrak (paper I). The fecundity, calculated as number of fertilized eggs, increases with female carapace size in the size range of 113-190 mm CW (figure 8). In this size range the fecundity is between 0.5-2.5 million eggs. Dry weight of egg mass to body mass ranged between 5 and 28 % (average 13 %, SD ± 5). The egg diameter (m) was independent of the number of eggs per batch or female carapace width.

Figure 8. Fecundity of female edible crab in the Kattegat and the Skagerrak (n=39) (Paper I). A larger female carry more fertilised eggs.

Histological examination of gonads Macroscopic gonad classes can be, especially the juvenile and adult undeveloped classes, classes

24 24 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) difficult to discriminate. In addition, the classification can be dependent on the observer. For this reason, histological analyses of the gonads in relation to the macroscopic classification were tested (Sjöström 2003). This study was the Master thesis of Elisabeth Sjöström, under supervision of Lillemor Svärdh and me. The objective of this study was to use histology, to classify the development of the gonads in female edible crab into maturity indices. In addition, we analysed if the macroscopic visual judgement of the gonad maturity reflected the physiological maturity of the ovaries. The gametogenesis (gonad development) of the females is divided into three main phases: the previtellogenesis and primary vitellogenesis which are continuing processes during the reproduction life of the female; and the secondary vitellogenesis which takes place during the reproduction season (Charniaux-Cotton&Payen 1988; Krol et al. 1992). By studying these phases six histological maturity indices were created (A, B, C, D, E and F). The histological indices A to E indicate a gradual development from the previtellogenesis to the late secondary vitellogenesis stage whereas F is a resting stage. Male crabs in the macroscopic group “developing” were histologically analysed, searching for sperm production of the testes, and sperm storage in the collecting tube and vas deferens. This group is critical, because it is difficult to macroscopically determine the maturity stage of the gonad (scenario 1 and 2 in paper I). In total, six macroscopic classes of the female gonad (n=13, in totally 78 samples), and 20 replicates of developing male gonads (three organs per individual, in totally 60 samples), were analysed. The samples were paraffin-embedded and stained by haemotoxylin- eosin, and analysed under light microscope. In addition to maturity indices, the mean oocyte area (n=5) was calculated for the female samples.

An increasing oocyte area in maturity indices C-E was observed indicating a change in physiology. The distribution of maturity indices differed statistically between groups macroscopically determined as primary (class 1/5) and secondary vitellogenesis (classes 2, 3, 3+, respectively) (figure 9). The figure 9 is a modified classification of Sjöström (2003), where I have re-classified some individuals e.g. to the resting stage F. However, macroscopic determined groups close in maturity stage did not differ in distribution of maturity indices, but they did differ in oocyte area. All males were physiologically mature.

Figure 9. Distribution of histological maturity indices A to F of the macroscopic female gonad classes 1 to +3. The classification is a modified version of Sjöström (2003).

The most important result from this study was that the histological analyses gave insight into the gonad development at the cellular level of both females and males. Therefore, I had better confidence in the forthcoming macroscopic classification, on which most of paper I rest. The macroscopic classes 1, 1/5 and 2 are regarded as undeveloped immature stages whereas classes 3, 3+ and 5 are regarded as mature. For males, the macroscopic three grade scales (immature,

25 25 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) developing, mature) were still used despite the fact that I now knew that the mid class was physiologically mature.

Longevity and natural mortality Sheehy and Prior (2005) estimated chronological age and corrected for thermal differences on the basis of cohorts modes of neurolipofuscin concentration frequency distributions (NCFD) for different areas with different mean temperatures, and not by use of individuals of known age reared in laboratory (Belchier et al. 1998). They showed that longevity varied inversely with sea temperature: longer life at the cooler East coast of UK compared to the warmer English Channel but the average maximum life span is around 10 years for edible crab within UK (Sheehy&Prior 2005). 95% confidence interval for age determinations of 1, 7 and 15 years are: 0.6-2, 5.2-9.7 and 11.8-19.7. In paper V we estimated the age of a large sized edible crab of 200 mm CW, using the L 217 and K 0.160 as in figure 6, to 19.2 years.

The importance of an accurate estimate of natural mortality is well known in fisheries assessment, and well known is the difficulty estimating it. A review of six common methods for estimating natural mortality (M) is given in Quinn and Deriso (1999): 1) catch curve analysis, 2) length frequency analysis, 3) mark-recapture experiments (Siddeek et al. 2002; Frusher&Hoenig 2003), 4) collection of dead organisms, 5) fitting population models and 6) meta analysis of life history. An alternative to estimations of natural mortality especially in data-poor populations is to use estimations for the same species but in other regions, or from other species with similar life history (alternative 6 above). This value is of course dependent on the accuracy of that estimation and how similar the taxa life histories are. General formulas, relying on parameters such as age at maturity, longevity, body size, L and K, often measured in biological studies, have been established (reviewed in Hewitt et al. 2007). We estimated (paper V) natural mortality from Pauly (1980) formula using L, K and mean habitat temperature, to 0.26 and using Rikther and Efanov formula (1976) based on age at maturation, to 0.18-0.34. Sheehy and Prior (2005) estimated natural mortality to 0.45 for males and 0.39 for females in UK East coast, based on Hoenig (1983) general formula using the oldest 5% for the average longevity.

The natural mortality is caused by predation on juveniles and sub-adults by codfishes and wolf fishes and by sea birds such as herring gull (own shell observations at skerries during summer). Hallbäck (1998) analysed the stomach content of fishes, and from this study it was shown that almost 50 % of the wolf-fishes Anarhichas lupus had pieces of edible crab <100 mm CW in their stomachs. Pieces of edible crab were also found in stomachs of cod Gadus morhua. Larger crabs are more safe to predators but on the other hand mortality caused by moult, inter-actions in mating activities and age senescence may increase with age.

Stock structure

The geographic area of the thesis The climate of the studied geographic area has changed over time as the Northern Europe have repeatedly been covered by ice to varying degree during Pleistocene era (1.8 Mya-10 kyr) of the Quaternary period: the British and Scandinavian ice sheets, respectively, covered land and shelf edges (~200-400 m depths) during glacial periods 500 000 years ago to that the last ice age melted around 9000 years ago. The ice sheets were possible confluent during last glacial maximum (LGM) approx. 20 000 ago i.e. ice covered central and northern North Sea region

26 26 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) which otherwise seem to have been ice free (Sejrup et al. 2005). The South Western ice limit of the British ice sheet is not fully agreed on but the northern parts of the Celtic Sea was covered. This knowledge is good to have in mind reading the about the population genetic structure (paper III) in this chapter.

The postglacial oceanography of Skagerrak, i.e. from 14 kyr to 8 kyr, is described by Gyllencreutz et al (Gyllencreutz et al. 2006). The ice margin, drainage and the circulation in Skagerrak and adjacent basins are presented in four time-slice maps covering the basal changes during this time period. During this time the present anti-clockwise circulation and the marine conditions has been strengthened mainly due to an increased impact from Atlantic marine water inflow and the North Jutland Current. A calving ice front was present in the northern and eastern flanks of Skagerrak while the ice was retreating 14.0 kyr ago; a northward freshwater current from the Baltic Sea existed already 14.0 kyr ago but thereafter changed in strength. At 11.2 kyr glacial meltwater from Närke strait reached Skagerrak trough outlets on the Swedish west coast (Otteid-Stenselva, Uddevalla and Göta Älv outlet). The modern circulation system was essentially established at 8 kyr when the eastern North Sea coastlines had attained present appearance. In the presentation of paper IV below and in the logbook part, the effect of the calving ice fronts and the moraine deposits upon the edible crab density can be seen in the geographical landing distribution.

Even on a shorter time-frame it is obvious that the climate in northern Europe and particularly in the North Sea is related to the warm and saline Atlantic waters to the region. This can be seen in “The Medieval Warm Period”(MWP) (AD 700-1350) during strong Atlantic water advection and “The Little Ice Age” (AD 1350-1900) probably caused by weaker Atlantic water advection. The oceanography of Skagerrak during the last 2000 years, has been analysed by sediment cores from different locations within and outside Skagerrak (Hebbeln et al. 2006). At AD 900 during the MWP an increase in the to Skagerrak inflowing bottom current occurred (and which is still persistent), explaining the seen lowered surface salinity as an increase of regional North Sea evaporation and a consequential continental precipitation (Hebbeln et al. 2006).

Today the prevailing surface current along the Swedish west coast is northward (Rodhe 1996). The baroclinic northward coastal current (the Baltic current) is more pronounced in Skagerrak than in Kattegat due to 1) the Kattegat-Skagerrak front forcing this low-saline water to contract along the Swedish coast, 2) as a result of the basic cyclonic current around the Skagerrak and 3) the often strong westerly currents towards the Swedish coast from north Jutland (Gustafsson&Stigebrandt 1996). The surface salinity is gradually decreasing in Kattegat possibly limiting crab larvae survival, and the reduction in salinity also penetrates deeper down negatively impacting adult edible crab.

Background stock structure A prerequisite for resource management of commercially exploited fish and shellfish species is to define how the resource is partitioned, spatially (geographically) and temporally, i.e. to identify stock units. As for species and population concepts there is no universally accepted definition of what constitutes a stock and there has been a shift towards an adaptive holistic approach admitting the use and need for several purposes (Begg&Waldman 1999; Carvalho&Hauser 1999; Waples&Gaggiotti 2006; Abaunza et al. 2008). All attempts of stock definitions struggle with optimizing a balance on precision and generality, and common words in the definitions are “self- sustaining”, “integrity/sharing”, “spatial/area” and “temporal/time” (Cadrin et al. 2005). In contrast to the species or population concept, there is an underlying meaning of management in

27 27 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) the stock definition. Different methods to investigate the stock unit have been suggested, which all have their strengths and weaknesses and often reflect the definition chosen by the investigator. The advantage of using a holistic approach is that one of the techniques may detect stock structure where others fail to do so. For example, morphologic or phenotypic traits for stock identification can be biased by environmental modulation so that separate stocks may be indistinguishable due to similar selection effects while at the other end of the spectrum directional selection may lead to false estimates of stock heterogeneity.

Genetic markers are powerful tools for describing population/stock structure (Utter 1991 ; Carvalho&Pitcher 1995). A major benefit of population genetics to fisheries management has been to define the concept of ‘stock’ in an evolutionary meaningful way, and to promote the use of this concept in management (Ihssen et al. 1981; Allendorf et al. 1987; Carvahlo&Hauser 1994). While gene flow is expected to promote genetic homogeneity, populations that are not exchanging genes are expected to acquire differences in frequencies of genetic variants over time by genetic drift. Therefore, by characterising the distribution of genetic variation, population substructuring can be detected and the degree of connectivity among populations estimated (Nesbo et al. 2000; Ruzzante et al. 2000; Hutchinson et al. 2001).

Movements – Paper II The dispersal ability of a species is related to that species’ population structure (Bohonak 1999), so that higher dispersal ability in general is associated with decreased differentiation, e.g. as measured by genetic distances, among populations. Consequently, knowledge of the dispersal processes during the entire life cycle of a species i.e. larval dispersal and the juvenile/adult life style may give an estimate on the geographic distribution of a population and the connectivity among populations (Jennings 2001; Hellberg et al. 2002).

The dispersal potential of larvae depends on the biology of the species (e.g. larval type, larval development time, hatching season and vertical migrations), and on the regional oceanography (e.g. directional currents, topographic gyres and cross shelf currents) and hydrological parameters (temperature, salinity). The distance of dispersal as an adult differs according to the life-style: benthic and sessile, benthic and non-sessile, or pelagic. A non-sessile species has the potential to disperse over geographic areas, also as an adult. At the extreme, larval dispersal and adult movement can interact and result in a high dispersal, or counter-interact and result in a relative low gene flow despite high dispersal potential for both larvae and adult.

To be able to manage exploited resources such as crabs it is important to have knowledge of how e.g. fishery in neighbouring or even distant areas impact the area in question. A limited larval dispersal and/or limited adult movement decrease the connectivity between areas, which opens for self-sustaining and in the long-term genetically heterogeneous stocks. In this case recruitment comes from within the area i.e. the area are vulnerable to the exploitation within the area and to less extent from outside. This situation, if exploitation is too severe, can lead to collapse of the resource and extinction of this genetic stock. However if exploitation is optimised yield can be high. Larger larval and adult dispersal make the stock structure less distinct and areas can work as recruitment sinks or sources, or both, complicating the management strategy. On the other hand, this stock structure is spreading the risks of collapse and extinction i.e. not all eggs are put in one basket.

In paper II we report the movement pattern of sub-adult and adult edible crabs on the Swedish west coast. We present previously unpublished data from a tagging experiment in the late 1960s

28 28 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) and movement data from a recent tagging experiment in 2003. The recent experiment use other areas for release compared to the initial but also one area in common. Acoustic tracking of males was also performed in 2005 to gather information on short-term movements. We specially investigate sex-specific differences in distance, direction and rate of movement, and analyse whether migration occurs seasonally, and whether it is size-dependent. Also we investigate the movement pattern of repeatedly recaptured individuals. The movement pattern is compared between areas and between studies i.e. 1968-73 and 2003.

Three marking methods were used in the mark-release experiments: The crabs in the initial experiment were marked with numbered plastic discs posteriorly attached by a braided terylene thread through two pierced holes in the carapace epidermal suture. In the recent experiment t-tags were inserted through a 2 mm drilled hole in the epidermal suture, and eight cm numbered plastic bands hung out and could be externally observed (figure 10, left). This type was used at the offshore and inshore Kattegat area. Black cable ties with yellow numbered discs tightened around the merus segment of the 1st periopod (claw) were used as a mark in the Skagerrak (area Strömstad and Fjällbacka) and the northern Kattegat (area Tistlarna) (figure 10, mid). The tagging procedure took mainly place aboard the fishing boats directly after capture and the crabs were released within two hours, in close vicinity to the place of capture. In total 3749 crabs were released in the initial experiment, from three Skagerrak locations, and of these 33 % were recaptured. In the recent experiment 8110 crabs from five locations were released, and 8 % of these were recaptured. In addition, nine males were tracked by the use of acoustic tags in 2005 (figure 10 right). Distance and direction of movement of recaptured crabs were calculated in the GIS programme ArcView 3.2.

Figure 10. Tagged crabs with floy t-tags, cable ties and acoustic tags. The tags were used in the mark-recapture experiment in 2003 and acoustic tracking in 2005 (Paper II). Photo: Anette Ungfors.

Females moved on average 6.4-21.7 km and males 1.5-8.8 km (averages within different areas, table 2). Female long-range movements > 5 km were predominately towards north and south from Strömstad, Fjällbacka and inshore Kattegat; towards south from the Brofjorden, Lysekil and Tistlarna and towards east from the offshore Kattegat release area. For males the direction pattern was uniform in most cases: e.g. the location Strömstad, Brofjorden, Tistlarna and inshore Kattegat did not differ from a uniform distribution in long-ranged movements. 78 % and 62 % of the female movements longer than 20 km from coastal areas were towards south, whereas 22 and 33 % were toward north and less than 5 % in eastward or westward direction (initial (ntotal=162) and recent (ntotal=58) study respectively). In the initial experiment females moved longer distances in October and November compared to July and August, and in the recent experiment the crabs moved longer distances in August compared to June. There was no difference in

29 29 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) movement distance between different sized females or males in either of the experiments. The rate of movement within six months was significantly higher than rates of crabs recaptured after a longer time period and females moved faster than males in both the initial (1968-73) and the recent (2003) experiment.

Table 2. Migration distance per area for a) the1968-73 study and b) the 2003 study (paper II).

Females Males

Mean±SD Median q25-q75 max n Mean±SD Median q25-q75 max n a) 1968-73 study Fjällbacka 12.6±23.1 2.5 0.8-10.6 137 32 1.5±4.1 0.6 0.1-1.7 36 197 Brofjorden 13.4±20.7 5.9 2.2-11.5 117 12 3.4±5.9 1.4 1.0-2.7 28 22 Lysekil 13.3±24.2 2.8 1.2-10.1 228 380 2.1±5.0 1.1 0.3-2.4 60 193 b) 2003 study 9 Strömstad 12.6±21.2 5.2 2.3-10.8 130 11 3.2±4.4 1.7 1.0-3.1 18 38 Fjällbacka 11.6±17.7 3.5 0.9-17.2 121 121 4.9±11.4 0.6 0.2-3.3 59 77 Tistlarna 21.7±22.7 7.7 6.0-43.3 71 35 3.2±1.9 3.5 1.1-4.7 6 13 Katt Insh 16.2±17.1 12.1 3.9-18.1 72 38 8.8±11.1 2.6 1.2- 32 13 Katt Offsh 6.4 3.5 1.5-5.6 44 15 3.9±6.0 2.5 1.5-3.8 40 80 6

Several hypothesis to explain migration patterns for Cancer spp. have been presented: inshore migration for moulting, mating and spawning, and offshore hatching migration (Diamond&Hankin 1985), migrations toward exposed area for spawning (Smith&Jamieson 1991), mating migration or pre-hatching emigration to avoid osmotic stress (Orensanz&Gallucci 1988) of C. magister, feeding migration in C. novaezelandiae (Chatterton&Williams 1994) and female migrations related to moulting and mating in C. pagurus at the north east coast of Scotland and England (Mason 1962; Edwards 1979). The extensive westerly or south-westerly migrations in the English channel (Bennett&Brown 1983; Latrouite&Le Foll 1989) are against the prevailing eastern-directed Channel current (Dahlgaard 1995; Guegueniat et al. 1995). Bennett and Brown (1983) point out that this may be an offshore migration towards grounds suitable for spawning and/or counteracting larval drift, and therefore having consequences for the replenishment of eastern stocks in the Channel. Robinson et. al. (2003) found strong indications of return movements of tagged edible crabs from the North west of Ireland. A large bulk of the recaptures (recovery rate approx. 37 %) moved north and westward to the continental slope but later south and eastward, back towards the release area. The crab movements from the south east of Ireland did not follow the hypothesised pattern of a against current movement but rather the opposite (Robinson et al. 2003). Northward movements of female crabs along the English east coast have been concluded by many investigators (reviewed in Edwards 1979), and a southward larval drift impacting recruitment further south have been assumed until recently. Eaton et.al. (2003) review larval investigations in the area and point at an aggregation of zoea I larvae offshore, south east of a front system separating areas to the north and south of a circulation gyre. This finding challenge the belief in that crab fishery in the south is dependent upon northerly spawning areas, and state that the offshore Dogger Bank may be a separate self-sustaining stock.

The prevailing surface current along the Swedish west coast is northward (Rodhe 1996). A northward dispersal of pelagic larvae could be the underlying reason for the observation that adult females predominantly migrate toward the south when distances over 20 km are considered. Dispersal of crab larvae for two months by a one-directional current of 0.20 m s-1 mean velocity (Rodhe 1996) move the larvae more than 1000 km downstream of hatching location. This distance is certainly a substantial overestimation of the true dispersal as the direction of currents

30 30 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) may change on daily basis and larval swimming behaviour, not least vertical migration (Harding&Nichols 1987; Park&Shirley 2005), will impact the realised dispersal distance. In our larvae simulation for 21 days (see Life History Chapter) the mean larval dispersal was 63 km, and most of the larval dispersal was to northeast, towards the Swedish coast from the offshore release spot in Kattegat (figure 4). Female adult migrations from offshore Kattegat were commonly towards E or NW. However, the calculation and dispersal simulation may indicate the need for a evolved behaviour, such as the upstream migration of females prior hatching or larval swimming behaviour (Shanks&Brink 2005), to guarantee continued recruitment along the Swedish coast.

Several mark-recapture experiments in Norway have been undertaken. Gundersen (1977) conducted experiments around Bergen and concluded that females moved more frequently than males, the major part of the movement were in southerly direction against the residual water movement and the longest distance moved was 37 km but most of the recaptures were taken within one year. Woll (1981; 1995) marked crabs offshore and in the fiord system around Midsund (N63°), mid Norway. The recaptures in these studies showed that females moved longer distances whereas males were more stationary. The offshore recapture rate was low but a single female, which moved longer than 1 km from the release area, moved towards southwest against the prevailing current. However, recaptures in the fiord system, with deep depths (200-299 m) to the south, were towards east or north east. Karlsson and Christiansen (1996) observed and tagged edible crabs in shallow areas below 5 m depth on a rocky islet on the southern Norwegian coast in Skagerrak. Edible crabs were not observed before May in this shallow habitat but then the authors clearly showed that the crab had a diurnal vertical movement as they observed many more crabs on their night dives compared to the day. The size of the crabs ranged from 50-190 mm CW, with an average of around 120-130 mm. Besides interesting findings on short term vertical feeding movement, Karlsson and Christiansen (1996) also found that males were more prone to stay in the area whereas females moved away to a larger extent. None of the males moved more than 3.5 km away but females were recaptured up to 28 km from release point. 61 % of the female movements were towards northeast (towards the Oslo fiord, against the prevailing current) and 39 % towards southwest.

Population genetics – Paper III The basic methodology for population genetic analyses is that individuals are sampled from different potential stocks, and the larger the genetic variance between samples the more distant their genetic origin. To diminish the risk that the marker is under selection or that the alleles are inherited in a non-Mendelian manner, several loci of the same marker or several marker types need to be used.

In general, marine species are expected to show weak population structure over large geographic areas due to fewer physical barriers, compared to land, and high dispersal ability via larval drift and/or adult movements (Ward et al. 1994). However, intra-specific genetic analyses of commercial decapods have revealed complex patterns of genetic differentiation at various geographical scales. Thus, the genetic structure of marine species is determined by the complex interaction of several factors including adult mating and pre-spawning behaviour, larval development time and behaviour, oceanography and its seasonal and annual variation, and must be empirically examined to inform management.

Sampling of individuals for genetic analysis (paper III) was performed at two different geographic locations within the study area and during different years in order to study the genetic allele variation on a geographic and temporal scale. In addition, a Norwegian sample from outside the area was analysed. 70 individuals were sampled at each occasion. The sampling of

31 31 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) crabs in Kattegat was performed in 2001 and 2007 at Groves bank (N57°06, E11°31), and samples from Skagerrak were obtained in 2002 and 2006 at Lunneviken (N59°03, E11°10). The third “outside area” location, a coastal location in the Norwegian Sea Norway called Midsund (N62°40, E06°40), was sampled in 2004. Eight microsatellite DNA loci were amplified with PCR. Screening and statistical analyses were by common methods, described in detail in Paper III.

The spatial and temporal genetic differentiation of edible crab is low within 1300 kilometres of waterway distance in the investigated area. This conclusion is supported by i) low global multilocus FST of 0.002 and non-significant single locus FSTs using allele frequencies, ii) non- significant global FST, single locus FST and pair-wise comparisons using genotype frequencies, (iii) no genetic differentiation among groups in AMOVA and (iv) that statistical power analysis suggested > 93 % power for our sampling design to detect an overall genetic differentiation of FST 0.002. Altogether, these results suggest that the genetic variation over a 1300 km water distance, from the basin of Kattegat at 57°N to the Norwgian Sea 62°N is very low. The cause of this low genetic variation, between groups of individuals over 1300 of kilometres, can be by a high gene flow or caused by large and young stock in the areas under low genetic drift, further discussed below.

Firstly, the lack of spatial genetic differentiation can be explained by a high gene flow over large areas. Female edible crabs are capable to move 100´s of kilometres and the pelagic larvae can disperse over long distances. A hypothesis explaining the pattern and cause of migration of females states that migration is directed towards the prevailing surface current to compensate for larval dispersal (Bennett&Brown 1983). This migration pattern opposite to current direction is valid for some areas, but not for all. Mark-recapture experiments in Kattegat and Skagerrak (paper II) demonstrated a large fraction of long southerly directed migrations of females from some coastal locations, thus against the coastal northward surface current, but also long migrations both northward and southward from other locations. There is a lack of knowledge concerning return movement or natal homing behaviour for the edible crab, which is described for other species in connection with spawning. But there are some observations indicating return movements for the edible crab (Robinson et al. 2003 and paper II), which could explain the northward migrations according to the hypothesis. If the above hypothesis is true, this could result in local genetic populations as the larval dispersal is compensating for the adult migration. Though, the results in this study indicate that adult migratory behaviour vs. oceanographic currents does not genetically structure the population in this area, undermining the above compensating hypothesis. Adult and larval drifts seem to cause high gene flow, diminishing genetic variation over a large area.

Secondly, the low genetic differentiation among the individuals within the studied geographic area may reflect historical gene flow persisting among recently founded large populations. The edible crab distributed in Kattegat, Skagerrak and mid Norway at present could have been re- colonised from an area south of British ice sheet e.g. English channel – Bay of Biscay or possible from a refuge in the North Sea. In this case, the time that has past is likely insufficient for genetic differentiation based on genetic drift. This especially applies for a large population typical of the edible crab (high density, high fecundity), as opposed to a small population where bottlenecks and stochasticity can change the allele frequencies over time to a larger extent.

32 32 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Spatial and temporal variation in phenotypic traits Phenotypic traits can be used as an indication of stock structure. A variation in a phenotypic trait between crabs from different fishing grounds may indicate a reduced stock interaction between different grounds. However, the variation in the trait can be caused of differences in the environment such as temperature, food and predator availability, or by differences in the density of edible crab. I was interested to investigate if the traits size distribution and moult cycle of edible crab differed at geographic locations. The moulting of adult edible crab takes place during summer-autumn but anecdotal evidence suggests that there are spatial differences in the timing of moult. The size data are also used in stock assessment (paper V), in addition to the purpose of using size frequency for stock identification. To sample this detailed fishery biological data, which is not acquired by the logbook system I involved fishermen for data sampling in 2002- 2004. In order to investigate a wider size frequency, three pots without escape gaps were given to each of 15 commercial crab fishermen. In addition to the standard pot, the fishermen would use three pots of their own design normally used in the commercial fishery. The reason to use the two gear types was to study the impact of the escape gap on the capture. The fishermen were told to record sex, carapace width measured to nearest mm and the moult status of the crab would be classified to a four-grade scale separating Newly moulted, New-moulted some time ago, Inter- moult of good quality and Degrading carapace. The fishermen were informed to use the standard pots within a normal string at their common fishing grounds and that they would measure the capture every time or a minimum 1-2 times per months. Except for the possibility to sell the capture in the additional pots each fisherman was given about 100-150 per year if a minimum of measurements was met.

The number of occasions that the capture in the pots were recorded as well as the data quality, varied between fishermen. A few fishermen filled out the protocols a sufficient number of times for both standard and commercial pot design, and a few more were filling out for one or the other of the two. The period for sampling was from within a short time period of a month or two, or was stretched across the season from May to December. Measurements to the closest cm were used in some cases, not to mm as told. Presentations of size frequency for different areas are given in figures 11-12. For comparison of size frequency between standard and own commercial pot design (with escape gaps) examples are given in figure 13-14. The size frequencies in some of the geographic locations may be questioned, especially where data are poor. There is a risk that not all crabs caught in the pots were measured e.g. to decrease labour. Unfortunately the data on the moult status are difficult to interpret. Most fishermen have filled out this column, but the variation of shell status is low. This can be caused by that the sampling process did not cover the main moult period or by uncertainties in the classification. New-moulted occurred during all season with a weak increase in September-October, no matter location.

33 33 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Figure 11. Size frequency in the catch of edible crab inshore and offshore Kattegatt for females and males, using standard pots without escape gaps. The data are from 2002, 2003 and 2004.

Figure 12. Size frequency at different fishing locations in Skagerrak, using standard pots pots in 2002 and 2003. Lunneviken (n=980, 18- 20 occasions, July/May to October), Pater Noster (n=572, 20 occasions, in July and August), Smögen (n=180, 11 occasions, 10th of July-19th of October).

34 34 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Figure 13. Size frequency of edible crab inshore Kattegatt for females and males, using commercial pots with escape gaps. More distinct increase in the capture frequency for crabs > 120 mm CW compared to standard pots without gaps.

Figure 14. Size frequency in standard and commercial pots in 2003 at two Skagerrak locations: Pater Noster (nstandard=446 at 18 occasions and ncommercial=379 at 19 occasions between 17 July th to 19 of December) and Smögen (nstandard=182 at 16 occasions June-October and ncommercial=72, 6 occasions, September-October).

It is less common for voluntary logbook sampling programmes to gather size data. Cooperation requires liaison and information to fishermen as fishermen suspect that the information can be used against their interests such as implementing quota or other enforcements. In addition, Starr and Vignaux (1997) compared size frequency of New Zealand rock lobster from logbooks and research sampling and found that there was a tendency for higher frequency modes (possibly

35 35 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) excluding smallest lobsters) in voluntary logbooks and larger frequency modes in research sampling. The designing and evaluation of length-frequency surveys for pot fisheries are discussed by McGarvey and Pennington (2001). They show that it was more efficient to sample one pot from all trips instead of several pots from a few trips. The variance between fishermen accounted for a relatively large part, and the least efficient sampling strategy was by research sampling measuring all pots on selected trips. Similar findings came from a Norwegian research project with detailed log book data (fishermen partly refunded) collected over 4 years by a reference fleet of professional fishers reporting the edible crab catch from four standardized trial pots set among their ordinary pots (Woll et al. 2006). Catch rate, catch composition, discards and size distribution was recorded, and the most efficient survey design is a collection of relatively small samples from many boats to reduce the between-vessel component of variation.

My conclusion is that it would be inappropriate to use the above sampled data on size and moult timing as phenotypic traits to distinguish a possible stock structure in Swedish waters. Possibly the size frequency difference between inshore and offshore Kattegat indicates some stock structuring but this difference can also be caused by larger mature crabs of the same stock inhabiting offshore areas. The size frequency between gears with and without escape gaps can possibly be seen as some higher proportion of crabs smaller than 120 mm in the standard gears. To improve the edible crab data sampling strategy in Sweden there is 1) a need to increase the refund per fisherman or call for an alternative incentive for co-operation, 2) possibly shorten or restrict the sampling period, 3) possibly decrease the pot number, 4) use only standardized pot, possibly with escape gaps, 5) increase the effort for information and instructions of each fisherman taking advantage of organization meetings etc as fishermen in general are not fond of written instructions, and 6) change to weekly reporting rather than annual.

Status of the Swedish edible crab stock

Density estimations – Paper IV In paper IV we present an estimate of the total abundance of adult crabs on the Swedish west coast, based on a combination of experimental fisheries to get catch per unit effort data and effective fishing area, and GIS modelling of available crab habitat. Fishery-related data, e.g. catch per unit effort (CPUE), is often used as a substitute for direct density assessments for estimating trends in stock size. In order to translate CPUE data from static gear e.g. baited crab pots to stock biomass or number, it is necessary to know the catchability coefficient q also defined as effective fishing area, i.e. the area from which all individuals of the target species are caught in one pot if the pot was 100% effective at catching crabs. In a mark-recapture experiment we estimated the effective fishing area around crab pots targeting edible crabs. Crabs were caught and marked at 5 locations in the Kosterfjord, Swedish Skagerrak coast in September 2003. Crabs were then released at 5 distances (10-160 m) in four directions from a baited pot. The number of marked crabs caught in the baited pot was then followed daily for 5 consecutive days. The current speed and direction close to bottom during the experimental period was measured daily with a drift buoy. In total, 1635 crabs were marked, and 45 crabs were recaptured (2.8%). The effective fishing area q was estimated to 2293 ± 1137 m2 (mean ± 95% confidence interval), corresponding to a circle with a radius of 26.6 ± 6.3 m.

In a separate experimental fishery during June and August 2003in the Fjällbacka archipelago located approximately 35 km south of the Kosterfjord, we estimated catch per unit effort at two depths strata (15-18 m and 25-30m) at 7 locations. CPUE did not differ significantly between seasons or depths, but differed significantly among locations. Using the effective fishing areas

36 36 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) estimated as described above, we calculated an average density of 0.0038 ± 0.0015 crabs/m2. Using GIS data on depth and sediment characteristics of Skagerrak and Kattegatt we calculated the area of suitable crab habitats along the Swedish West coast. We defined a suitable crab habitat to be between 10 and 40 meters water depth, and with a bottom consisting of bedrock, stone, gravel or sand. The area of suitable crab habitat was estimated to 4142 km2 (figure 15), which combined with density estimates from Fjällbacka would indicate that the catchable population of crabs on the Swedish west coast would be approximately 16 ± 6.3x106 crabs.

Figure 15. The suitable crab habitat (10-40 m depth and bedrock, stone, gravel or sand) is estimated to 4142 km2 (grey in sea). Landing positions for crab pots, net and fyke-nets in 2004- 2007 are also given.

Stock assessment – Paper V Crustaceans repeatedly shed their shell for growing and the lack of a structure showing annual growth marks makes it difficult to age individuals. However, age determination by lipufuscin pigment is promising (Tully 1993; Sheehy&Prior 2005). Still, the age determination of crustaceans must be considered expensive and time-consuming but age- length keys have recently been used in parameter estimation and stock assessment (Sheehy&Prior 2005; Fonseca&Sheehy 2007). Below I present short descriptions of some available and used stock assessment methods for crustaceans, mainly based on Smith and Addison (2003).

General production models or Biomass dynamics models, assume CPUE to be proportional to stock abundance. Input data is a time-series of catch and effort data, and the data are more informative if data cover a wide range of biomass and effort levels. These models provide estimates of reference points such as the maximum sustainable yield (MSY), fishing mortality at MSY (fMSY), and biomass at MSY (BMSY). Available free computer programmes are e.g. ASPIC (http://www.sefsc.noaa.gov/mprager/aspic.html) and COLERAINE (http://fish.washington.edu/research/coleraine/).

Depletion models are based on how the removal (catch) influences the remaining abundance. CPUE are often used, and are assumed to be proportional to population size. The classical models assumes a closed population with no immigration or emigration, and predicts how large cumulative removal should be to reduce the abundance to zero, which is then an estimate of the current population abundance. If used on unexploited or early in a fishery developmental phase, the reference point unexploited biomass is estimated. Variability in catchability (q) is of particular concern when the methods are applied to crustaceans (Miller 1990). Frusher et. al. (1998) recommend that the method should be restricted to fisheries with high exploitation rate and relatively uniform size composition over the area. Stock assessment of the Irish edible crab have been performed by an open population depletion model considering soak-time, using a tagging experiment with an intense effort of recovery (ICES 2003). Soak-time is the time that the hauled gears were deployed at sea.

37 37 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Length-based population analyses are sex and size-structured abundance estimating models using the probability of moult and increment for different size cohorts, gradual increased recruitment potential (egg production) over length and if possible are spawning-recruitment relationship are included so that recruitment can be calculated. Fishing and natural and handling/discard mortality are often the factors decreasing the cohort abundance (Zheng et al. 1995; Punt&Kennedy 1997; Zheng et al. 1997; Siddeek et al. 2004). These models offer a high degree of biological realism but are computationally complex, and need supporting input data on biological processes e.g. as growth, maturity, natural mortality and of fishing processes as catchability and selection.

Length cohort analysis (LCA) produces fishing mortality and abundance estimate per length class. Input data are length frequency of the catch from a population assumed to be in equilibrium (i.e. no trends in recruitment or mortality/exploitation), growth parameters K and L and natural mortality. In LCA the parameters of growth rate is important as von Bertalanffy growth curve (VBGC, relation of size with age) is used for estimation of the taken time (t) it takes to grow between cohorts (Jones 1990), instead of using 1 year as in virtual population analysis (VPA) or age cohort analysis (ACA). The model works from the largest to the smallest cohort to calculate the cohort abundances that must have been at start of the time period accounting for the assumed natural mortality and the estimated fishing mortality from landing data. The reliability of length cohort analyses and the shortcomings of the model have been discussed (Hilborn&Walters 1992). Efforts on minimizing the model limitations i.e. the discrepancy between size and age have been made by excluding the largest cohorts with too large variation in size-at-age, and by including sensitivity analyses of growth parameters and natural mortality (Jones 1979; Addison&Bennett 1992). Still, LCA is used for relative comparison of yield per effort with different growth parameters (Ulmestrand&Eggert 2001) or used for its simplicity and lack of alternatives (Wolff&Soto 1992; Kirchner 2001).

In paper V we assessed the stock of edible crab in Skagerrak and Kattegat with length cohort analysis, using von Bertalanffy growth parameters L and K estimated from length frequency data and mark-recapture experiment. Input data length frequency of the catch removal (landing and discard) is shown in figure 16. The calculation steps of LCA were describe in Jones (1984) and a recent user-friendly description of length cohort analyses was presented by Jennings et al (2001, p. 143-144). The impact of different parameters on stock indicators i) fishing mortality, ii) current stock abundance (numbers and weight) and iii) and egg production of the spawning stock have been analysed. Monte Carlo resamplings of L, K, weight-at-size and fecundity-at-size were used to estimate the sensitivity on stock indicators of input parameter. The analyses were made in Matlab 7.5 (MathWork Inc.). In addition to the commonly used value of natural mortality of 0.2, we ran the LCA for natural mortalities of 0.1 to 0.3 to cover a likely range of this parameter.

Figure 16. Raised landing frequency for females anandd males in the Kattegat and the Skagerrak. Used in stock assessment in Paper V.

38 38 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

The fishing mortality was higher for females than for males (figure 17), and the fishery in Kattegat exploits larger individuals whereas the fishery in Skagerrak seems to have a wider exploitation pattern. The mean fishing mortality Fall and the Fp are around 0.3 for females and 0.2 for males. Overall, the fishing mortality seems low. Based on total commercial and estimated recreational landing of 403 tonnes in Kattegat and Skagerrak, the estimates on the current stock ranged between 1600-2600 tonnes or 4-8 million of edible crabs, and the egg production was around 5-7x10^11 eggs. These ranges of stock estimates are based on different values on growth parameters, weight-size, fecundity and natural mortality. A lower natural mortality generated a lower stock abundance and egg production whereas a higher natural mortality generated higher stock indicators. Natural mortality had an impact on the estimated fishing mortality, such as a lower natural mortality resulted in higher fishing mortality.

Figure 17. Skagerrak. Fishing mortality (mean ± 95 % confidence interval) of a) females using L 217±12.2 and of b) males using L 217±8.6. 1000 runs (paper V).

Logbooks Licensed Swedish fishermen fill out mandatory logbooks. In 1994 when Sweden became a member of the EU, a logbook of a common type was introduced in the Swedish fishery. Skippers on fishing vessels over 10 m length have to report fishing activities on daily operational basis whereas skippers on vessels below 10 m fill out journals on a monthly basis. The daily logbook type is more detailed and useful for assessment as the number of gears and effort hours are given. Gear effort is not given in the monthly journals but the number of fishing days for that month as well as landing per day. The data quality in the logbooks has improved over the years but still e.g. the number of gears could be reported in a more accurate way.

To give a picture of the edible crab fishery in Sweden, logbook data from 2007 are presented in more detail: The total landing is 148 540 kg, and of this 80 966 kg (55%) is taken by crab pots. Nine fishing vessels over 10 m are targeting crab with pots with a total landing of 27703 kg and 12704 pot hauls i.e. a rough estimate on LPUE is 2.18 kg/pot. Using this landing rate an estimation of the pot hauls for vessels under 10 m are estimated to 24432 pot hauls. The total effort of fishermen targeting crabs is then 37136 pot hauls in a year. The LPUE for 1995-2007 is given in figure 18 (left graph) based on daily logbook reporting, and since 1999 onwards there is no trend in LPUE using data for Kattegat and Skagerrak. LPUE since 1999 is on average 2.22

39 39 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) kg/pot excluding 2000. However, the LPUE per area is more variable but since 2004 the LPUE in both areas seem to be stabilised around 2.0-2.5 kg/pot. I have not been able to get effort data from 2004-2005.

Figure 18. Left graph show annual LPUE in 1995-2007 based on daily log-book reports of vessel >10 m. Right graph show LPUE (kg/pot) in 2007 for vessels >10m for soak-times up to one week.

Catch or landing per unit effort can be used as an indicator of the stock abundance. However, several factors in addition of stock abundance can affect the LPUE. The abundance of crabs is higher on certain grounds, and the search behaviour of fishermen to optimize yield may provide trends in CPUE that do not reflect real changes in abundance. Generalized linear models can be used to quantify the variation in LPUE by e.g. year, month, area, soak-time and vessel/vessel type e.g. Bell et. al. (2005). GIS information can elucidate variation in LPUE in logbooks due to differences in depth and substrate. Based on capture position given in the Swedish logbooks, the geographical positions of the landings plotted on depth and substrate type, respectively (figure 19) indicate that landings mainly occur in shallow areas composed of mixed substrate. Other factors are trap saturation and soak time. Many traps within an area may decrease the catch rate, or as trap saturation commonly means: that the capture in a trap impacts the further catch (Miller 1990). Catch rate is increasing with prolonged soak-time at least up to some asymptotic level defined by the gear design. Logbook data in 2007 for vessels over 10 m length showed how soak- time affected the catch rate (figure 18, right graph). The soak-time (days) shows a positive correlation with catch rate. Soak-time up to 7 days are included, catch rates after approximately 10 days of soak time decreased probably due to crab escapes or misreporting. In this data both one and two chamber pots are used (no discrimination in logbooks, which further could improve the data set). A two-chamber pot fish differently compared to one-chamber: escapes by time are prohibited or at least decreased in the two-chamber pot by a soft entrance into the extra room. This means that high capture rates in two chamber pots can camouflage decreases in stock abundance.

40 40 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Figure 19. Fishing positions in the commercial edible crab fishery in 2004-2007. Left graph show depth strata and right graph substrate strata in the Kattegat and in the Skagerrak.

To improve stock assessment the compilation of fishery data is most important. Logbooks can be used to assess the stock by e.g. surplus biomass models or by analyses of trends in LPUE. A time-series of logbook data over an approximately 10-20 years might be needed, and the input data should mirror the absolute abundance. The existing logbook system is fully comparable to other EU countries, and in some cases even better as even the small vessel tonnage (< 10 m) are reporting on monthly basis. However, there is need for better guidance in how to properly report, in particular the effort columns. The exact numbers of hauled pots, not an approximation or a rounded off number, should be given. To be able to standardise the LPUE for soak-time, information on effort hours must be reliable. For more detailed knowledge of the capture such as sex ratio and size frequency, a new license system for the coastal segment can build on agreement of co-operation of the licensed fishermen to sample necessary data. Earlier research on how to efficiently sample a reliable length frequency clearly recommends to sample few pots from several to all fishing vessels instead of sampling a larger amount of pots from a few vessels or by occasional observer sampling (McGarvey&Pennington 2001; Woll et al. 2006). The pot type should be of similar standard design to exclude different catch rate caused by dissimilarities, and as two-chambered pots may camouflage stock decrease one-chambered standard pots might preferable be used.

41 41 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Conclusions

SWOT In this section I combine old and recent (this thesis) knowledge in a somewhat subjective SWOT (Strengths-Weaknesses-Opportunities-Threats, table 3) analysis of the fisheries and biology characteristics of the Swedish edible crab stock. By this operation I wish to illustrate and summarize the advantages or drawbacks of the stock status, potential management strategies as well as the gaps in our knowledge.

Today we know the life history of the Swedish edible crab to varying degree: relatively much is known of its adult migration potential (paper II) but less is known about larval dispersal and natural mortality, the latter most important for stock assessment (paper V). The stock might extend over large geographic areas in the range of 1000 km (paper III) but the possibility for some local smaller stocks cannot be excluded. Genetic population analyses on crabs in UK showed that close locations could be significantly different (pair-wise comparison) despite no genetic isolation-by-distance (no diversification with distance) (McKeown&Shaw 2007). Significantly different close locations always included an inshore area, and complex oceanographic features promoting local retention that could affect larvae from these areas. The fecundity is high (paper I) but on the other hand the larval development period is long (months), so a large proportion of the hatched larvae does not to settle. Maturity occurs relatively late, at an age of 5-8 years. The escape gap size needs to be increased to 90 mm to be consistent with the recommended MLS of 140 mm (paper I).

The two independent estimations of stock abundance (paper IV and V) came up with estimates not so far from each other: in the range of 10-22 million crabs (95 % CI) in paper IV and 4-8 million crabs (95 % CI, different parameter values) in paper V. However, the confidence intervals are not overlapping. Both estimates are impacted by several factors such as catchability, parameter values (e.g. natural mortality) and assumptions (e.g. about suitable habitat, or that length can be used as a cohort). As the total landing of edible crab most probably is under- reported the abundance estimate in paper V is too low which mean that most confidence should be put on the higher estimate.

Stock status is judge to be in a sustainable condition, and even to have the potential to be exploited to a higher degree. For now, before e.g. age-based or length-based models have further improved the assessment level, stock assessment can be based on indicative LPUE assessment. This means that in case the LPUE declines this needs to be followed by management restrictions. For this option, logbook data need to be reliable, as stated before, to be able to explain changes in LPUE due to changes in abundance or due to e.g. changes in fishery distribution or other change in exploitation pattern.

42 42 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Table 3. A SWOT-analysis of the exploitation and management of the Swedish edible crab stock. STRENGTHS WEAKNESSES OPPORTUNITIES THREATS

Fisheries • Selective gear • Local trap • Marketing of • Fishing on • Low benthic saturation; Swedish edible crab, female soon to impact Competition of also males spawn fishing grounds •Product development • By-catches of (diversification) berried females •Potential increased in nets landings • Used as bait •Promotion of high • Claw market quality crabs by light • Mortality on sorting device soft crab e.g. for claws or poor handling Life history •High gene flow •Natural • Relatively late • Low mortality? sexual catchability of •Larval dispersal? maturation berried females • Catchability? • Longevity • High fecundity Stock structure • One • Different stocks homogenous in short term stock in long- ecological term evolutionary perspective? perspective Stock • Low fishery •Reliable stock • Age determination • Unreported assessment mortality assessment? by lipofuscin used for catches (e.g. in • 15-30 % harvest • Length frequency assessment crab pots, rate (F110-160) vs. age frequency? • ICES WGCRAB lobster pots, fish • Stable LPUE •Logbook Assessments nets and misreporting recreational fishery) Management • Escape gaps • No minimum • Co-operative • Present escape landings size management gaps too small • No monitoring •Protection of except logbooks spawning areas • Poor effort • MLS 140 mm CW reporting in •Prohibit handling logbooks, better mortality of soft and guidance needed berried females • Pot type? Stock status •Under-exploited • Area not fully •Un-reported •Increasing stock exploited mortality and (fishermens removals observations) •Low predation due to low abundance of e.g. codfishes

43 43 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Local management of edible crab One of the aims of this thesis is to evaluate on what geographic level the Swedish edible crabs should be managed. This implicitly means to estimate the geographic distribution of the stock and equal this with the management unit. Of the many available stock definitions I base the conclusion of stock distribution on population genetics where low genetic variation is considered to occur within one stock. With the information we now have, Kattegat and Skagerrak can be looked upon as one homogenous stock, and therefore should be treated as one management unit. However, does this argument exclude local management such as local co-management of fisheries, implementing smaller management areas than the stock unit?

Laikre et al (2005) discuss three types of genetic population structures in relation to fishes in the Baltic Sea, namely distinct, continuous and no differentiation. They conclude that local overexploitation, or even extinction of populations with no differentiation, may not have a serious effect on total genetic variation in comparison with the two other genetic population structures, as long as the effective population size is large enough to counter the effect of genetic drift. However, the ecological effect could be serious. Therefore, local management of the edible crab can be considered and implemented if stakeholders take a precautionary approach such as implementing size restrictions and not fishing below a certain local biomass. However, local over harvest does not severely impact the total genetic pool, as long as no extensive fishery exists on all local management areas and as long as corridors for genetic connectivity between them prevail.

Co-management initiatives limiting fishermen entrance, can the decrease the open access of the resource and by this can build an increased responsibility of the participating fishermen (Shotton 2002; Piriz 2004; Brady&Waldo 2008). Symes (2007) put the light onto different questions that need to be considered in establishing co-operative organisations. However, increased yields or revenues can repay sound resource exploitation of the participating stakeholders. As the stock status of the edible crabs within the co-management area also depends on recruitment and mortality in other areas, as well as immigration and emigration, the stock may not recover from depleted conditions in spite of a sound local fishery. However, as long as this is understood and that fishermen are monitoring the resource and react (adaptive management) if negative trends occur or if limits of negotiated reference indicators such as fishing mortality or stock biomass are reached, smaller management units than stock distribution is practical. Communication between co-management areas needs to be established to tune the overall exploitation. Also, marine protected areas in the Kattegat and Skagerrak, working as a recruitment source or as a precautionary strategy, can be one way to safeguard against failures.

44 44 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Research perspective To use an alternative modelling strategy such as dynamic length-based method (Punt&Kennedy 1997), we need to evaluate the available data. Biomass surplus modelling (Hilborn 2001) using LPUE data and landings from logbooks can be worthwhile and can be tested with data from 1995-2007. The LPUE in the logbooks can be improved by detailed review of the reported effort through e.g. interviews with skippers to get information on the amount of used gears over the years, and possibly to get private landing records. Generalized linear models can be used to quantify the variation in LPUE by e.g. year, month, area or vessel/vessel type. Variation in LPUE in the logbook due to differences in substrate or habitat can be elucidated by available position of fisheries and GIS information.

Establishing age-length keys for the Swedish edible crab is a tempting prospect. The calibration to chronological age and the thermal correction of age estimates for edible crab were made on the basis of cohorts modes of neurolipofuscin concentration frequency distributions (NCFD) for different areas with different mean temperatures (Sheehy&Prior 2005), and not by use of individuals of known age reared in the laboratory (Belchier et al. 1998). If pronounced temperature differences between Kattegat and Skagerrak fishery locations, keys need to be established for both areas as Sheehy and Prior (2005) found a strong relationship between sea temperature and neurolipofuscin accumulation rate.

As the knowledge of the juvenile crab distribution in Sweden is scarce it would be interesting to investigate if the Laminaria habitat also is a nursery area for the edible crabs in Sweden.

Within the thesis I tried to evaluate the fishery-dependent estimates of the crab densities by use of remotely operated vehicle (ROV). This ROV study can be worth re-evaluation with an increased filming effort or by use of divers or underwater cameras (UWTV) on sledge.

The genetic analysis can be extended to include more locations, such as samples from the inner fiords.

Estimates on natural mortality need to be reliable for the use in assessment models. Research fishing in marine protected areas with no commercial fishery or in formerly un-fished areas, gives information on the natural mortality by length frequency analysis or catch curves (age) i.e. the total mortality = the natural mortality.

45 45 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

Acknowledgements (Tack) First I have to express the joy of having spend all these years at Tjärnö Marine Biological Laboratory since coming here as a student in 1997, then working as an marine biologist in Fishery Technology Centre (FTC), and later on as a PhD student and in projects for fisheries development. Many thanks to the TMBL first lady Kerstin Johannesson, my Idol when it comes to marine biology, speaking talent and combining-career-with-family-issues, and to her co-driver Lars Hagström and all the TA staff.

Then, folk responsible for that I came into the crab business is my supervisor Per Nilsson, a very busy man damn good at statistics, who could not possible has guessed that not one but two children later he got rid of me :=D. Colin Wheatley who put effort into crab development and me. Eva-Marie Rödström for being my mentor (now you know) and support in a lot of issues.

Hans Hallbäck, IMR/H-lab, has most kindly shared a lot of his earlier findings and data on the edible crab. I spend my first half a year as a PhD student plotting all the mark and recapture location in GIS, which meant I had to identify and find a lot of small local-named Islands along the Swedish west coast. After that I was pretty good at the name of all Islands. Later on I repeated this process with own data...Mats Ulmestrand, a fishery biologist knowing everything about lobsters, has been my direct channel to the Swedish Board of Fisheries (data bases), a colleague in SUCOZOMA and LCA mate. The meetings within the ICES Crab Working group where I have got the possibility to find out about ongoing crab research, have been invaluable. Many thanks to e.g. Julian Addison, Derek Eaton, Oliver Tully, Martin Robinson, Daniel Latrouite, Suzanne Henderson, Beth Leslie, Astrid Woll, Jan Sundet, Knut Sunnanå and many more. Astrid Woll at Möreforskning, Norway examplary in the co-operation with fishermen, thanks for all communication during the years about crab biology, meat yield, management and the comments on the thesis summary. Hope we can come up with a project together! In 2001 I attended the annual research expedition on the Red King Crabs in the Northern Norwegian Fiords, where Jan Sundet och Ann Merete Hjelset learned how to measure and mark big crabs 24 h per day for two weeks. Thanks for that experience!

Many thanks to my two master students Elizabeth Sjöström and Helena Sundström, and the colleagues Christin Appelqvist and Lillemor Svärdh not only for making me feel as a group member, but also for assistance during mark-recapture and reporting, experimental fishing and histological work! To all the VOF-group members and particular its shellfish- and wine loving chairwoman Susanne Lindegarth - soon I will have the best home-site ever! Later on I had use of my assistant supervisor Carl André, the DNA lab boss, thanks for your contribution. This last year, having the privilege to work in the DNA lab with all the EGG hang arounds was worth waiting for: Benno Jönsson learned me how to use the still functional ALF-machines and Anna- Karin, Marina, Rick, “Pia”, Tuuli, Johanna G and Petri all shared their knowledge about useful PCR programmes, pipetting etc. Marina also gave professional advices when working with the statistical analyses and commented the manuscript. Many thanks also to Niall McKeown and Paul Shaw for primer sharing and collaboration.

It is fantastic how many people that really have been involved in a thesis, this must be a true altruistic behaviour (ok some money has been transferred): Thank you Tomas Lundälv for ROV filming at shallow depths around crab pots with dangerous ropes :=), Jon Havenhand for language improvements (and other comments) in paper II, Roger Johansson and Sven-Gunnar Lunneryd for all help with the heavy acoustic buoys, Magnus Wahlberg for the acoustic tags, assistants in crab tracking Benno, Linus, Malin K. Many thanks also to Annika L, a new fast-

46 46 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus) working friend, and Frank S which I have pushed hard in Nephrops projects. Hans-G for corridor chatting.

All best friends and colleagues who I have shared years as “single” or as “married-wanna-be”, preparing fancy or simple dinners, in SPAs, drinking wine and chatting: Solveig van Nes for our friendship, for commenting on manuscript and summary, you are an excellent godmother to Amanda; Karin and Hasse for shared interests in a lot and for comments on the summary; Susanne and Mats L for hospitality among many other good characters; Malin and Jerry – looking forwards to more grill parties; Eva-Marie and Per for being you, and Per - thanks; Gunilla –sailing? Henrik you are doing a great “prefekt” job; Marina and Anita – garden planning evening?; Mia and Martin for lively discussions.

Och min allra bästa kojbyggarkompis Anna Nilsson för all tid vi har spenderat tillsammans, på cyklar, vid kiosken, på discon, tja vad har vi inte hittat på! Ditt telenummer används fortfarande “flitigt” när jag bara vill prata lite eller behöver peppas upp. Och alla grannar och andra barnfamiljer som lyser upp tillvaron under kvällar och helger: Ronny och Charlotta för att ni försöker få lika fin gräsmatta som oss; Håkan och Camilla som flaggar för oss; Malin och P-O som har våra barn hos sig; Roger och Helene som drar ut oss på minst en skogs-eller båttur varje helg; Anna och Gunnar för grillkalas.

Och tänk alla fiskare som jag tagit över rodret hos: Bröderna Patrik och Joakim och pappa Ingemar i Lejet, Martin och Folke i Bua, Per-Arne i Ringhals, Gilbert i Kullavik, Lennart i Marstrand, Henning och Lars-Erik på Tjörn, Bo på Orust, Björn i Fiskebäckskil, Henrik i Norra Grundsund, Martin på Smögen, Lars-Åke i Långasjö, Janne och Nisse på Resö, Morgan och Per- Gösta i Strömstad. Hallands Skaldjursutveckling EF med vildbasingen Viking Bengtsson. Tack alla ni och alla andra som lämnat in återfångstrapporter & andra observationer!

Och min Sturköfamilj då? Pappa John-Erik som bara måste ut på ”sjön” varje dag, och varifrån jag troligen har snappat upp intresset för havet, det är Dig jag ser framför mig när jag tänker på hållbart småskaligt kustfiske. Mamma Inga-Lill som är en viktig grundbult i familjen Ungfors, som har haft en viktig roll i fisket och som nu intagit en annan viktig roll – rollen som supermormor! Äldsta broder Anders med sin Kristina, mellanbroder John & Marie och Jessika, och så minstingen Martin med sin Caroline, finfina bröder och svägerskor som håller mig kvar i Ungfors-klanen trots långt avstånd oss emellan – tur att det finns telefon och datorer. Fast på sistone är det väl busungarna som ni helst vill prata med?

Min Strömstadfamilj då? Ja, dom har fått ta på sig rollen som min extrafamilj. Men om dom fattat vad jag håller på med – nej, det tror jag inte! I alla fall, tack till Majsan, Freddan & Ginny, Victoria & Robert och Putte & Mona för alla familjesammankomster, barnvakter och promenader. Men hur ska jag tacka min allra närmaste underbara familj? Niclas, den bästa pappan och livskamrat, som varit så förstående i alla fall de sista månaderna – du ska få spela bridge och åka på husvagnssemestrar så att du storknar under kommande år! Amanda och Malte, ni är alldeles för bra för att vara sant. Älskar Er!

My PhD study was supported by the Swedish research programme on Sustainable Coastal Zone Management, SUCOZOMA, funded by the Foundation for Strategic Environmental Research, MISTRA; The Department of Marine Ecology, University of Gothenburg; and Project Västkustkrabban, funded by The EU Economic Fond for Fishery. In addition, economic support for chemicals, field equipment and for participation in conferences have been given by Orvar and Gertrud Nybelin Fishery Fund, Helge Ax:son Johnson Foundation, Iris foundation, Kurt Belfrage Fund, Adlerbertska Research Fund, Wilhelm and Martina Lundgren Scientific Fund, Clara Lachmanns Foundation, KVVS, Colliander and Birgit och Birger Wåhlströms Foundation.

47 47 Anette Ungfors 2008 Fisheries biology of the edible crab (Cancer pagurus)

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Wolff M, Soto M. 1992. Population Dynamics of Cancer polyodon in La Herradura Bay, Northern Chile. Marine Ecology Progress Series 85, 69-81. Woll A. 2003. In situ observations of ovigerous Cancer pagurus Linnaeus, 1758 in Norwegian waters (Brachyura, Cancridae). Crustaceana 76, 469-478. Woll A, Emblem W. 2005. Size at sexual maturity of females brown crab (Cancer pagurus) in three regions in coastal Norway. ICES SCRAB REPORT 2005. Report of the study group on the biology and life history of crabs. 9-11 May 2005, Galway, Ireland. Woll AK. 1981. Krabbens (Cancer pagurus) biologi i midtre og ytre Romsdal. Title in English: The edible crab (Cancer pagurus) biology in Inshore and Offshore Romsdal. Master thesis in Marine Biology, Trondheim University. 75 pp. Woll AK. 1995. Resursbiologisk undersökelse av taskekrabben (Cancer pagurus) i Möre og Romsdal. Title in English: Resource biological investigations of the edible crab (Cancer pagurus). Möreforskning Ålesund Report to Norway Research Council/Norges Forskningsråd. 54 pp. Woll AK, Berge GM. 2007. Feeding and management practices affect quality improvement in wild-caught edible crab (Cancer pagurus). Aquaculture 269, 328-338. Woll AK, van der Meeren GI, Fossen I. 2006. Spatial variation in abundance and catch composition of Cancer pagurus in Norwegian waters: biological reasoning and implications for assessment. ICES Journal of Marine Science 63, 421-433. Zheng J, Murphy M, Kruse G. 1995. A length-based population model and stock-recruitment relationships for red king crab, Paralithodes camschaticus, in bristol bay, Alaska. Can. J. Fish. Aquat. Sci. 52, 1229-1246. Zheng J, Murphy M, Kruse G. 1997. Analysis of harvest strategies for red king crab, Paralithodes camtschaticus, in Bristol Bay, Alaska. Can. J. Fish. Aquat. Sci. 54, 1121- 1134. Østvik S, Grimsmo L, Schei M, Halvorsen J, Dauksas E. 2006. Utnyttelse av biprodukter fra krabbeforedling. Report in Norwegion. Title in English: Use of by-product from crab processing. RUBIN, Rapportnr. 4404/130. 23 pp.

55 55

318 Sexual maturity of the edible crab (Cancer pagurus)in the Skagerrak and the Kattegat, based on reproductive and morphometric characters

Anette Ungfors

Ungfors, A. 2007. Sexual maturity of the edible crab (Cancer pagurus) in the Skagerrak and the Kattegat, based on reproductive and morphometric characters. – ICES Journal of Marine Science, 64: 318–327. The size at the onset of sexual maturity of female and male edible crab (Cancer pagurus) from the Skagerrak and the Kattegat and the fecundity of females were estimated. Physiological maturity of females, i.e. ovary development, was at a larger size than behavioural maturity (indications of successful copulation). The carapace width (CW) at which 50% of females were mature (CW50), based on development of the gonads, was 132 mm, sperm presence gave a CW50 of 107 mm, and the presence of sperm plugs a CW50 of 118 mm. Changes in relative abdominal width were found at approximately 100 and 130 mm, and CW50 was 104 mm. A smaller fraction (25%) of the females is functionally mature at sizes ,140 mm. However, male physiological and functional maturity was more synchronized: CW50s based on advanced sperm production and allometric changes in the chelae were within 5 mm (117– 122 mm). Size-speciﬁc fecundity increases with CW (0.5–2.5 million eggs). Recommendations for a minimum landing size (MLS) of 140 mm and a change of escape gap size to 90 mm are given. Legislation of a MLS of 140 mm CW for females and males will reduce future potential landings more in the Skagerrak than in the Kattegat. Keywords: allometry, Cancridae, fecundity, gonad development, management, minimum landing size, size at maturity. Received 23 May 2005; accepted 24 November 2006; advance access publication 16 January 2007.

A. Ungfors: Tja¨rno¨Marine Biological Laboratory, Department of Marine Ecology, Go¨teborg University, S–452 96 Stro¨mstad, Sweden; tel: þ46 526 686 88; fax: þ46 526 686 07; e-mail: [email protected]

Introduction it is limited to the Skagerrak and the Kattegat, where there is a To avoid recruitment-overfishing of brachyurans, recruits to the small commercial fishery. The total landings in 2005 in Europe fishery should be able to reproduce at least once. To meet this were 46 280 t, most in the UK, Ireland, and France. In 2002, the requirement, management actions can restrict the size of landed Swedish landings in fisheries targeting crabs were 105 t, 57% of crabs by minimum landing size (MLS), by restrictions on the gear the total taken by crab pots, and of this, 68% (57 t) was caught by deployed, or by a one-sex harvesting strategy. Additional regu- boats ,10 m (ICES, 2003). In Sweden, the main landing season is lations can protect the pre-recruits and recruits at vulnerable July–November. In most parts of its distribution a MLS is stages of their life, e.g. by decreasing handling mortality during implemented, either of national (UK, Addison and Bennett, 1992; moulting periods by seasonal closures (Hankin et al., 1997; Norway, J-102-2004) or international status (Anon., 1998). Siddeek et al., 2004). The size at the onset of sexual maturity However, the crab fishery in Swedish waters in the Skagerrak and (SOM) needs to be considered in the implementing process of a Kattegat is not regulated by implementation of a MLS, but by MLS, and signs of mating activities, gonad development, or allo- obligatory 75 mm escape gaps in pots fished shallower than 30 m metric changes in growth of the body parts have been used to dis- and in fykenets fished deeper than 10 m (Anon., 1998, 2004a). criminate between juveniles and adult Brachyura, e.g. Cancridae These escape gaps allow crabs of carapace width (CW) ,110– (Weymouth and MacKay, 1936; Edwards, 1979; Brown and 120 mm to escape (Dybern, 1983). In the northern part of Bennett, 1980; Campbell and Eagles, 1983; Orensanz and Gallucci, Skagerrak, from the Swedish border to the Norwegian southwest 1988; Orensanz et al., 1995; Hankin et al., 1997; Pinho et al., coast (Rogaland), the commercial landing of crabs ,110 mm is 2001), Portunidae (Gonza´lez-Gurriarań and Freire, 1994; Muino prohibited (Anon., 2004b). et al., 1999; de Lestang et al., 2003; Hall et al., 2006), Majidae The aim of this study is to investigate whether the current (Alunno-Bruscia and Sainte-Marie, 1998; Sampedro et al., 1999), management actions in the Skagerrak and the Kattegat preclude and Xanthidae (Flores and Paula, 2002). Stock assessment can use recruitment-overfishing. The SOM is defined as the CW at which egg production (S) of mature individuals and stock-recruitment 50% of the population is mature, and both physiological and relationships of commercial species (Addison and Bennett, 1992), functional sexual maturity are considered by evaluating the so for management purposes the relationship between size and gonad development in both sexes, the presence of sperm plugs egg production (fecundity) is important. and filled spermathecae in females, and by measuring male chelae The edible crab (Cancer pagurus) is distributed along the and female abdomens. I did not sample ovigerous females for Northeast Atlantic coast (Christiansen, 1969): in Swedish waters, maturity because of their low catchability (Howard, 1982).

# 2007 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. For Permissions, please email: [email protected] Sexual maturity of Cancer pagurus in the Skagerrak and the Kattegat 319

However, I did conduct fecundity analyses, so that they can be considered in the process of MLS recommendation and in stock modelling. In addition, I experimentally evaluated the potential for crabs to escape from creels with gaps of different diameter and forecast the potential commercial landings under an MLS based on the SOM.

Material and methods Sampling and classification From July to December of 2001 and 2002, edible crabs of both sex were collected from fishing vessels (potters) operating in the Figure 2. Claw of the edible crab (Cancer pagurus) and archipelagos along the Swedish Skagerrak coast and on coastal morphometric measurements. RPL is the right propodus length, and RPH is the right propodus height. The right propodus width (RPW) and offshore banks in the Kattegat (Figure 1). Subsamples of the is not shown but is measured at the widest part of propodus. catch were brought to the laboratory. As reproduction of Cancer Modified from an illustration by H. Samuelsson, Go¨teborg spp. has a temporal component (Charniaux-Cotton and Payen, University, Sweden. 1988; Shields, 1991) females for ovary classification were sampled from September to December, when a large proportion of Cancer pagurus females have ripe or ripening ovaries (Edwards, 1979). plugs in the oviducts of early post-moult females. CW, female Ovaries were classified as immature (previtellogenesis), undeve- fifth abdominal segment at the broadest part (AW), and the loped (primary vitellogenesis), developing (early secondary length, height, and width of the male right propodus (RPL, RPH, vitellogenesis), ripe/mature (late secondary vitellogenesis), or and RPW, respectively) (Figure 2) were measured to the nearest resting (primary vitellogenesis, loose appearance), and testes were millimetre. If the right chela was missing or regenerating, the left classified as immature (no visual indication of, or just tiny 5 mm propodus was used (a pairwise t-test showed no significant coiled, testes), developing (production of spermatozoa has difference between right and left measurements of RPL, RPH, or started, testes and vas deferens are thin but partly filled), or RPW; p ¼ 0.07–0.41, n ¼ 34). Moult stage was determined mature (vas deferens is extended and filled by a white mass according to four classes: (i) crabs at early post-moult, having a of spermatophores). Observations were made on the presence of soft carapace, a whitish appearance and sharp toe tips; (ii) crabs spermatophores in the spermathecae and the presence of sperm with indications of recent moulting, i.e. a clean appearance but not fully hardened shell (late post-moult); (iii) inter-moult crabs had some fouling organisms, worn toe tips, and a presumed high meat yield; (iv) crabs with shell necrosis and many fouling organisms were classified as degrading. This classification is not based on Drach’s (1939) setal definition of moult stage (A–D4), but rather on a modification of macroscopic characters, e.g. as used by Edwards (1979).

Analysis of size at sexual maturity SOM was estimated by fitting the percentage of mature crabs per 5 mm size interval to the logistic equation Proportion 2 mature ¼ 1(1 þ Ae(BCW)) 1 by non-linear least squares regression (Somerton, 1980). The CW at which 50% of crabs are mature (CW50), i.e. the mature proportion P ¼ 0.5, is calculated as 21 CW50 ¼ 2log AB . Females were defined as mature if the ovary was in a developing or mature stage during autumn, or if there were indications of mating (e.g. the presence of sperm in spermathecae or a sperm plug in early post-moult females). For males, two alternative scenarios for gonad classification were applied in the calculations: gonads classified as developing were defined either as immature (scenario 1) or as mature (scenario 2), because there were definition difficulties with this stage. Chi-squared tests were used to analyse differences in the mature proportion of inter-moult and post-moult females and males and the mature proportion of females in autumn and summer. The allometric relationship between size (CW) and organ dimension (AW, RPL, RPH, and RPW) was analysed in three ways: (i) a one- or two- phase model (Gaertner and Laloe´, 1986), (ii) minimum sum of squared residuals (SSR) in the transition zone (Lovett and Felder, Figure 1. Sampling areas for the edible crab Cancer pagurus for 1989), and (iii) iterative assignment of adolescent individuals analyses of SOM (black circles) and for ovigerous females for (Somerton, 1980). Data were divided into two data sets, juveniles fecundity analyses (crosses). or adults, on an a priori basis. For (i), the lower a priori limit for 320 A. Ungfors female adults (LA) was set to 150 mm because 75% of large affects the size of potential escapements. Four escape gap sizes females have developed or resting ovaries (this study). Further, (75, 80, 85, and 90 mm) were tested against six different size three limits for juveniles (LJ) were used, namely ,104 mm (100% classes of crabs (115–119, 120–124, 125–129, 130–134, 135– immature), ,109 mm (75% immature), and 124 mm (75% 139, and 140–144 mm CW). Four females and four males per undeveloped). Most males .110 mm CW are mature in the UK size class were arranged within a creel placed in a tank (Edwards, 1979), so an a priori higher LJ males was set at 109 mm, (9 1 0.7 m) with circulating water (11–138C, salinity 33). and for adults at 110 mm. A priori limits for (ii) and (iii) are Three creels per tank were used (in separate compartments), and provided graphically. bait (fish) was hung on the outside of the creel. Over 10 d, all Ovigerous females for fecundity analyses were collected in possible combinations were tested twice, in random order and April and May 2002. Samples (n ¼ 29) were collected as bycatch with eight creels per night. The proportion of escapes per size in nets deployed for lumpfish (Cyclopterus lumpus) west of class and escape gap was calculated. Ma˚seska¨r (588040N118180E) at depths of 40–50 m, or in crab The future Swedish edible crab landing potential if a MLS is creels at Kummel Bank (578280N118230E) (n ¼ 10) in the implemented from the SOM results of this study was estimated. Kattegat (Figure 1). After fixation for 1 month in Davidson Five alternative values of MLS were simulated for females (the solution (Lightner, 1996)), the egg mass was washed in water, four calculated CW50s plus one precautionary), and five alterna- separated from pleopods, and dried to constant weight at 608C. A tive values of MLS for males (the three CW50s plus two precau- sample (n ¼ 10 per crab) of fixed but not dried eggs was measured tionary). The percentage of the landing potential compared with for oocyte diameter (mm). Three subsamples of 2–10 mg (0.1 mg recent capture (%, numbers of crabs) without implementation of accuracy) of approximately 200–650 eggs were chosen randomly a MLS but an escape gap of 75 mm was calculated for females and for exact enumeration and calculating egg weight per subsample. males, respectively, on the assumption of MLS being knife-edged, The whole crab was dried to constant weight in four main pieces, and from data on the sex-specific size frequency in commercial and the total body weight was recorded. The weight of the missing catches. The data on crab size composition in commercial catches claw (or claws) was calculated from the regression equation were gathered at different sites along the Swedish coast between y ¼ 0.342x – 31.23 (n ¼ 39, r2 ¼ 0.86, p , 0.0001; model with 1999 and 2003: (i) females in the Skagerrak (Stro¨mstad, n ¼ 4112; best fit of data), where y is the dry weight per claw and x the CW. Fja¨llbacka, n ¼ 1842; Lysekil, n ¼ 363) and the Kattegat (offshore Losses of walking legs were considered by additions of a mean Groves Bank, n ¼ 2259; inshore Varberg, n ¼ 465) and (ii) males walking leg weight or by the regression equation y ¼ 0.4886x– in the Skagerrak (Stro¨mstad, n ¼ 1743; Fja¨llbacka, n ¼ 1642; 43.5 (n ¼ 35, r2 ¼ 0.91, p , 0.0001), where y is the dry weight of Lysekil, n ¼ 705) and the Kattegat (offshore Groves Bank, four pairs of walking legs and x is again the CW. Fecundity (the n ¼ 710) (Figure 1). number of fertilized eggs per crab) was calculated by dividing the total dry weight of the egg by the mean weight of each egg (the standard deviation was calculated by triplicates of egg Results weight). Relative fecundity was calculated as a proportion of the The proportion of females with a developed ovary (developing or dry weight of eggs and body. Fecundity and relative fecundity mature) was 41% during summer and 64% during autumn were analysed statistically by linear regression (untransformed and (x2 ¼ 47.1, p 0.001, n ¼ 920) (Figure 3). The ovaries of logged data) and by testing the curve fit to logarithmic, quadratic, 30–50% of females of intermediate size (124–149 mm CW) were power, exponential, and logistic relationships, respectively (using in a resting stage in summer, compared with ,25% in autumn. In the computer program SPSS), with CW used as a measure of body autumn, most females of intermediate size were in an undeve- size. The relationship between oocyte diameter and the number of loped stage, but irrespective of season, larger females (150 mm eggs per batch and with CW was tested by linear regression. CW) were generally classified as mature. Most crabs in CW classes A manipulative laboratory experiment was set up in October 124 mm were immature and undeveloped. During autumn, the 2005 to determine how the diameter of the escape gap in creels proportion of females with developing or mature ovaries was

Figure 3. Ovary stages during (a) the summer months June–August (n ¼ 521), and (b) the gonad development period September– December (n ¼ 399) of crabs in 5 mm CW intervals (endpoint of interval shown). The data are based on inter- and post-moult crabs. Sexual maturity of Cancer pagurus in the Skagerrak and the Kattegat 321

Figure 4. The proportion of mature female edible crabs based on (a) developing and ripe ovaries during autumn (n ¼ 399), (b) the presence of sperm in the paired spermathecae (n ¼ 1128), and (c) presence of a sperm plug in the oviduct of early post-moult (n ¼ 446). Logistic growth curves are drawn (parameters presented in Table 1). The CW50 is 132, 107, and 118 mm, respectively. higher for inter-moult (80%) than for post-moult females (51%) 95–104 mm CW and a second minimum at 125–139 mm CW (x2 ¼ 35.1, p 0.001, n ¼ 399). (Figure 6a). Minimum total SSR was at 125–129 mm CW for The proportion of mature females based on the reproductive male length propodus (RPL), and at 119–124 mm CW for male characters, ovary development, spermathecae, and sperm plug height propodus (RPH) (Figure 7, inset). presence increased with CW (Figure 4). CW50 is 132, 107, and The CW50 based on morphometric data was 104 mm for 118 mm, respectively (logistic regression, Table 1). The general females (Figure 6b, Table 1) and 122, 122, and 120 mm for male patterns of gonad development for inter-moult and post-moult RPL, RPH, and RPW, respectively (Figure 7, Table 1). Dividing males were similar (Figure 5a, b), but post-moult males were data into juvenile and adult groups based on an iterative process more often classified as immature or developing (52%) than fitted the linear regression better than the pooled data set (AW inter-moult males (26%) (x2 ¼ 44.4, p 0.001, n ¼ 631). The F ¼ 529.9 p 0.05; RPL F ¼ 306, p 0.05; RPH F ¼ 515.8, proportion of mature males based on gonad development per p 0.05; RPW F ¼ 464.8, p 0.05). The growth coefficient of 5 mm CW size class increased with CW (Figure 5c). CW50 was adult female AW decreased, whereas the juvenile and the male 117 mm if a developing gonad was considered immature, and chela (RPL, RPH, and RPW) showed greater positive allometry 101 mm if it was considered mature (Figure 5c, Table 1). during adult growth (Table 1, coefficient B). The 95% confidence A two-phase regression model fitted the allometric data better interval did not overlap between juvenile and adult phases for than a one-phase model for both sexes: the SSR for linear either variable (Table 3). regression of the two-phase model was lower than for a one-phase Fecundity, measured as the number of fertilized eggs, increased regression of juveniles and adult data combined (Table 2). The with female CW (linear regression r2 ¼ 0.68, and log-log linear total SSR on allometric data of female AW showed a minimum at regression r2 ¼ 0.71, p , 0.000, n ¼ 39; Figure 8a) in the size

Table 1. Regression (log Y ¼ log A þ B log CW) summary of the iterative assignment of morphometric data, where Y is abdomen width (AW), RPL, RPH, or RPL (log A1 and B1 ¼ juvenile phase; log A2 and B2 ¼ adult phase) of edible crab.

Sex and morphometry Log A1 constant B1 coefficient Log A2 constant B2 coefficient Log A constant B coefficient CW50 Females ...... Abdomen 21.8864 1.5986 21.4619 1.4152 224.2413 0.2337 103.7 ...... Spermatheca – – – – 219.034 0.1785 106.6 ...... Sperm plug – – – – 23.0957 0.0261 118.5 ...... Ovary – – – – 217.002 0.1289 131.8 ...... Males ...... RPL 21.280 1.276 21.9649 1.6033 28.0619 0.0666 122.5 ...... RPH 21.306 1.304 21.577 1.454 27.7268 0.0632 122.3 ...... RPW 21.245 1.185 21.588 1.357 27.1330 0.0597 119.5 ...... Scenario (i) – – – – 27.6669 0.0655 117.0 ...... Scenario (ii) – – – – 214.809 0.1468 100.9 2 The adult proportion of morphometric and reproductive data is fitted by non-linear least squares to the logistic equation: Proportion mature ¼ 1(1 þ Ae(B*CW)) 1 and the coefficients log A and B are given. CW50 is calculated from these coefficients (–log A/B). Two scenarios of maturity stage of male gonad are considered: (i) developing gonad treated as immature and (ii) developing gonad treated as mature. The iterative process fitted data in the CW range 100–149 mm for females and 94–149 mm for males to the juvenile or the adult phase. The method is based on that of Somerton (1980). 322 A. Ungfors

Table 2. Comparison of a one- and a two-phase relationship between AW and CW of females, and of RPL, RPH, and RPW and CW of males. Sex, size, and SSR1 SSR2 Fpd.f. morphometry Females ...... LJ ,104 mm 0.186 0.177 9.076 ,0.05 2 and 361 ...... LJ ,109 mm 0.199 0.187 11.904 ,0.05 2 and 375 ...... LJ ,124 mm 0.317 0.305 10.052 ,0.05 2 and 515 ...... Males LJ ,110 mm ...... RPL 0.079 0.075 3.22 ,0.05 2 and 125 ...... RPH 0.070 0.065 4.65 ,0.05 2 and 125 ...... RPW 0.095 0.092 1.97 ns 2 and 125 SSR1 is the sum of squared residuals when combining juveniles and adults to one phase, and SSR2 the same when splitting into two phases. Data of intermediate sizes (LJ–LA) are not included in the one-phase regression. The data ﬁt a two-phase linear regression better (F-statistic) than a one-phase regression (except for the data on RPW). The method is based on that of Gaertner and Laloe (1986).

The CW50 determined from the different biological characters may be used as background for implementation of a MLS in the Skagerrak and the Kattegat. The effect of different potential MLS (CW50) on the Swedish catch potential is shown in Figure 9. The simulated impact on the capture potential of females subjected to implementation of a 104, 107, 118, 132, or 140 mm CW as MLS led to a decrease in the number captured with increasing MLS in the Skagerrak and the Kattegat. The decrease was more severe in Figure 5. Gonad stages of (a) inter-moult (n ¼ 360) and (b) the Skagerrak (Koster, Fja¨llbacka, and Lysekil) than in the post-moult males (n ¼ 271) per 5 mm CW interval. Gonads were Kattegat (Varberg inshore, Groves Bank offshore). A MLS of classified as immature, developing, or mature on the basis of visual 140 mm in the Skagerrak resulted in an estimated local specific inspection of the testes and the vas deferens. (c) The proportion of capture potential of 33–57% of the present catch, but in the mature males per 5 mm CW interval. Treating the developing male Kattegat the result was a 80–87% decline. In Figure 9b, the simu- gonad as immature or mature gives a CW50 of 117 or 101 mm lated impact of 101, 122, 130, or 140 mm MLS on male capture ¼ (n 631). Logistic growth curves are drawn (parameters presented potential is shown. A MLS of 140 mm CW in the Skagerrak in Table 1). reduced the capture potential to 32–51%, and in the Kattegat to 80% of the present catch by number. range 113–190 mm CW. At that size range, fecundity was between 0.5 and 2.5 million eggs. Relative fecundity, calculated as the Discussion relationship between number of eggs and body weight, was inde- Size at onset of sexual maturity pendent of CW (linear regression, p ¼ 0.39) and fitted poorly to SOM of female edible crab in the Skagerrak and the Kattegat is in other models (r2 ¼ 0.02–0.07, p . 0.07) (Figure 8b). The accord with the results of maturity studies on the species in other relationship between dry weight of the egg mass and body weight European areas. Sperm plugs are observed in the gonadopore ranged between 5 and 28% (average 13%, s.d. +5%). Egg from 100 mm CW (this study) and larger in several areas diameter (mm) was independent of the number of eggs per batch (105–211 mm CW in the English Channel, Brown and Bennett, ¼ 2 ¼ ¼ (linear regression, p 0.197, r 0.044, n 39) (Figure 8c) or 1980; .107 mm Yorkshire data, Edwards, 1979), and CW50 based female CW (linear regression, p ¼ 0.278, r2 ¼ 0.032, n ¼ 39). The on sperm plug presence is close to our 118 mm (116 mm CW East mean oocyte diameter averaged over subsamples and crabs was Coast England, Edwards, 1979; 115–119 mm CW Shetland, m + 383 m (s.d. 20). The ovaries of all ovigerous females were Tallack, 2002a). A CW50 derived from observations of sperm in macroscopically classified as resting: a greyish loose appearance of the spermathecae has not been calculated before. However, our small ovaries in primary vitellogenesis. Only one ovigerous female results indicate that mating takes place at smaller crab sizes than showed signs on the carapace of recent moulting, i.e. it was rela- expected from sperm plug indices: the CW50 based on sperm tively soft and whitish; the rest had a hard carapace with fouling plugs is also likely overestimated, as shown in Figure 4c. The ovary organisms. The smallest ovigerous female (113 mm) had no develops at a similar body size in different areas of Europe. The sperm in the spermathecae, as did all other ovigerous females. CW50 of 132 mm in Swedish waters (this study) are comparable Escapements from creels with different gap sizes are shown in with the 130–134 mm CW at the Shetland Islands (Tallack, Table 4. The proportion of escapement of different size classes 2002a), the 127–139 mm off southwest Ireland (Edwards, 1979), indicate that a 90 mm gap is required to allow escapement of the and the 132–138 mm around Ireland (ICES, 2004). However, Le larger crabs in the experiment (135–144 mm CW). Foll (1986) reported a CW50 in the Bay of Biscay based on ovary Sexual maturity of Cancer pagurus in the Skagerrak and the Kattegat 323

Figure 6. AW in relation to body size (CW) of female edible crabs. (a) Minimum of SSR in the transition zone of females is observed at 99–104 mm and 129–139 mm. (b) Relationship between the logarithm of AW and the logarithm of CW for juveniles and adults (n ¼ 689). The division into mature adult females was based on Somerton’s (1980) iterative assignment and a priori LJ .104 mm and LA . 150 mm. The CW50 is 104 mm (Table 1). development to be as low as 111 mm (i.e. 73 mm CL). This may move the logistic curve to the left (signiﬁcant differences in gonad be an effect of living in southern parts of the species distribution, development between post- and inter-moults in autumn), result- where the water is warmer, and temperature does impact the size ing in a lower CW50, possibly explaining the geographical differ- at sexual maturity in other crab species (Fisher, 1999; de Lestang ences in ovary maturation. No CW50 has been reported for large et al., 2003; Defeo and Cardoso, 2004). In this study, the CW50 female crabs in the English Channel (Brown and Bennett, 1980), assessed from ovary development during autumn included both which borders the Bay of Biscay, but 85% of females .115 mm post- and inter-moult females: excluding post-moult crabs might (all size categories lumped together) had developed gonads in autumn (Brown and Bennett, 1980). A report from an ICES study group on crab biology and life history point to 130 mm CW as the SOM of maturity of female C. pagurus in the North Sea (ICES, 2003). However, the size distribution of ovigerous females (H. Hallba¨ck, unpublished data, q25 ¼ 142, q50 ¼ 152, q75 ¼ 162 mm, min ¼ 109 mm) in the Skagerrak and the Kattegat indicates that most females do not spawn until yet another moult. The size range of ovigerous females in the Skagerrak and the Kattegat is of the same magnitude as elsewhere in Europe: in the English Channel, ovigerous females range from 133 to 205 mm (mean 166 mm) (Brown and Bennett, 1980). The smallest observed ovigerous female from the English east coast was 129 mm CW, but out of 200 females examined, most that were ovigerous were .152 mm (Edwards, 1979). Pearson (1908) measured the smallest ovigerous female in northern parts of the North Sea at 115 mm. In situ CW measurements

Table 3. 95% confidence intervals of coefficient B in the linear regression log Y ¼ log A þ B log CW coefficient, where Y refers to measures of abdomen, right propodus length, right propodus height, and right propodus width, and CW is the carapace width. Dependent variable Y Juvenile B Adult B Figure 7. Logarithm of the RPL plotted against logarithm CW for Abdomen 1.565–1.633 1.390–1.439 ¼ ...... juvenile male and adult male edible crabs (n 509). The RPL 1.236–1.316 1.560–1.647 classification into mature males was based on Somerton’s (1980) ...... RPH 1.270–1.337 1.419–1.490 iterative assignment and a priori LJ .94 mm and LA . 150 mm...... The CW50 was calculated as 122 mm (Table 1). The left corner of RPW 1.147–1.223 1.315–1.399 the graph shows a minimum total SSR at 124–129 mm and 119– The confidence interval does not overlap between juveniles and adults of 124 mm for RPL and RPH, respectively. either variable. 324 A. Ungfors

Figure 8. (a) Absolute fecundity (number of eggs) plotted against CW, (b) relative fecundity (number of eggs per dry body weight) plotted against CW (mm), and (c) oocyte diameter of female edible crabs (n ¼ 39) in Swedish waters. Oocyte diameter (mm) is similar for large and small batches (linear regression, p . 0.05). Mean oocyte diameter is 383 mm (s.d. +20), the s.d. being based on three subsamples. of 16 ovigerous females of 122–159 mm at a site off northwest from other areas. Edwards (1979) observed male crab gonads Norway (Woll, 2003) gave an indication of the size of ovigerous from Yorkshire and southwest Ireland, and based on the presence females in Norwegian waters. Statistical analyses (minimum of of a ripe vas deferens, suggested that most males .110 mm were SSR) and graphical observations (Figure 6) of female allometric mature. Similar studies around the Shetland Islands suggest data indicate three cohorts: one with relatively steep allometric maturity (CW50) at 110–114 mm CW (Tallack, 2002a). The growth of the abdomen ,105 mm CW, one with relatively less CW50 in the Bay of Biscay is at about 102 mm (67 mm CL), on growth of crabs 105–133 mm CW, and one for larger crabs with the basis of histological analysis of gonad development (Le Foll, faster growth. Interestingly, Tallack (2002b) found a change in 1986). In the current work, classification of the gonads of inter- relative AW in females .100 mm, consistent with the present and post-moult males suggests that shell condition does have an findings of first minima at 95–104 mm and a CW50 of 104 mm. impact on gonad development (Figure 5). This finding is contrary Tallack (2002b) also noted that female pleopod capacity had an to that of other authors, who suggest that gonad maturation is not inflection point at 138 mm CW. This phenomenon is also affected by moulting (e.g. Edwards, 1979; Pinho et al., 2001), but observed in snow crab (Chionoecetes opilio; Alunno-Bruscia and a change during the year in male Cancer magister sperm content Sainte-Marie, 1998), those authors suggesting a downscaling in has been shown by Swiney and Shirley (2001). Enlargement of the the allometry of intermediate-sized crabs brought about by later male chela at 110 mm CW (the onset of maturity) is reported by structural limits on abdomen size. The size at which sexual matur- Edwards (1979), some 9–12 mm less than the CW50 of Swedish ity of females is attained covers a wide range. It seems that copu- male crabs assessed on the basis of morphometry. However, the lation takes place once the females reach 110 mm CW, and intersection point discriminating Shetland juvenile male crabs physiological maturity one moult later at around 130 mm CW, from adults is calculated to be 102–105 mm CW (Tallack, 2002b), but that fertilization needs yet another moult, at around 150 mm. a value conspicuously lower. Differences in methodology (inter- Findings on the size of mature male in the Skagerrak and the section vs. 50% mature) can explain some of the differences, but Kattegat (Figure 5, Table 1) reveal a similar size range as reported geographical differences in size at attainment of maturity cannot

Table 4. Summary of the edible crab escapement experiment of creels equipped with traps with gaps of different diameters (75–90 mm). CW (mm) 75 mm 80 mm 85 mm 90 mm Total (%) F M Total (%) F M Total (%) F M Total (%) F M 115–119 0 0 0 93.8 7 8 44.0 3 4 63.0 5 5 ...... 120–124 0 0 0 37.5 3 3 44.0 4 3 63.0 5 5 ...... 125–129 0 0 0 0 0 0 13.0 0 2 38.0 3 3 ...... 130–134 0 0 0 0 0 0 6.0 0 2 44.0 1 6 ...... 135–139 0 0 0 0 0 0 0 0 0 6.0 0 1 ...... 140–144 0 0 0 0 0 0 0 0 0 6.0 0 1 Four females (F) and four males (M) of each range of CW class were located within a creel, and each combination was run overnight on two occasions. The total proportion of escapes (%) are given per gap and CW class (n ¼ 16), as is the sex-speciﬁc number of escapes. Sexual maturity of Cancer pagurus in the Skagerrak and the Kattegat 325

Figure 9. Different hypothesized MLS and the resulting catch potential in the Skagerrak (Stro¨mstad, Fja¨llbacka, and Lysekil) and Kattegat (Varberg and Groves Bank) for (a) female and (b) male edible crabs. The number of crabs per area is given in the section Material and methods.

be excluded. Application of morphometric and reproductive data as fully mature. To reduce the risk of recruitment-overfishing, that considers the developing male gonad to be immature results landing restrictions on females could be introduced if based on in a CW50 at the higher end of these findings (117–122 mm CW). observations on the size-specific proportion of ovigerous crabs in However, interpreting developing gonads as mature yield a value the population. However, few egg-carrying female edible crabs are of CW50 at the lower end, close to a CW50 based on histological captured by the fishing gear (Edwards, 1979; Howard, 1982), and analyses in the Bay of Biscay. Campbell and Eagles (1983) con- female crabs in cold, temperate waters may not spawn annually sidered male gonads that were slightly developed to be immature, (Swiney et al., 2003), all of which results in sampling problems because of their low numbers and the small developing spermato- and biases. Other characters can be used as indicators for female phores. In summary, the onset of sexual maturity for males is at maturity analysis to overcome sampling problems and biases. size ranges between 100 and 120 mm CW, if based on the findings Physiological and functional maturity are not synchronized for herein and in earlier literature. females, but span wide ranges, and for this reason caution in Fecundity of the edible crab (0.5–2.6 million eggs, Figure 8a) instituting management action is needed. Further, fecundity is is in accord with findings in the UK (0.8–2.9 Million eggs; magnitudes higher for large females than for first-spawners, and 145–183 mm CW, Edwards, 1979) that show that fecundity ovigerous females are likely to have a higher CW50 than assessed increases with female size. Larger females not only have larger through physiological maturity analysis. For male crabs, physio- gonads, but their pleopod capacity, sperm content in spermathe- logical and functional maturity are more synchronized, and take cae, and AW increases with size (Tallack, 2002b). Any variation in place at smaller size. However, small physiologically and function- the fecundity between crabs caused by differences in the moulting ally mature male Chionoecetes opilio and Cancer gracilis rarely take stage (Hankin et al., 1989) or egg development (O’Clair and part in reproduction because of competition with larger males Freese, 1988; Shields, 1991) is probably small in this study because (Alunno-Bruscia and Sainte-Marie, 1998; Orensanz et al., 1995). all females (except one) were of similar inter-moult stage, there Also, the size of copulating males exceeds that of post-moult was no visible eye-pigment formation of the eggs, and the eggs females (Hankin et al., 1997), indicating copulation size limits for were of similar colour. In addition, the eggs were of similar size, smaller males. However, Edwards (1966) found that a 110 mm despite differences in absolute numbers per batch. However, male Cancer pagurus copulated with a 151 mm post-moult female fecundity standardized for body weight is similar for the females and that the sperm contribution of small male edible crabs was in the size range seen here (Figure 8b) and the egg mass to body less than expected from gonad and morphometric studies alone. weight ration was of similar magnitude to that of other species Maturity characteristics tend to be sampled by traps that may of the genus Cancer (11–19 %, Hines, 1991). The eggs of cancrid have underestimated the real CW50, because the proportion crabs are of similar size, and because of the large body size of the mature may well be higher in active than in passive fishing gear animals, the fecundity of cancrid crabs is among the highest (Smith et al., 2004). Precautionary management based on a poss- reported (Hines, 1982), especially that of larger females. ibly underestimated CW50, along with the diverse maturation process of the exploited edible crab stock in Swedish waters, Management recommendations and their effects results in a suggested MLS for females and males of 140 mm CW, on catch potential particularly if the crab industry develops and fishing effort bur- Hartnoll (1969) suggested that female crabs are mature when they geons. A legislated MLS of 140 mm CW would ensure that almost are capable of extruding eggs, and males when they can mate/ all of Swedish landings of male edible crabs are physiologically copulate successfully. This means that the crabs must be both and functionally mature, that 75% of female crabs are physiologi- physiologically and functionally mature before they can be treated cally mature, and that approximately 25% of female crabs are 326 A. Ungfors functionally mature. In other words, spawning is relatively intense References and fecundity fairly high, so even the larger female crabs may have Addison, J. T., and Bennett, D. B. 1992. Assessment of minimum accessibility to suitable mating partners. I assume that the MLS in landing sizes of the edible crab, Cancer pagurus L, on the East force in the English Channel (.140 mm CW) exceeds the size at Coast of England. Fisheries Research, 13: 67–88. which 50% are mature (Bennett, 1995). The MLS in neighbouring Alunno-Bruscia, M., and Sainte-Marie, B. 1998. Abdomen allometry, Norwegian water is just 110 mm CW south of 608N, and for that ovary development, and growth of female snow crab, Chionoecetes reason alone there seems to be reason for Norwegian authorities opilio (Brachyura, Majidae), in the northwestern Gulf of to reconsider it or to find other ways of improving management St Lawrence. Canadian Journal of Fisheries and Aquatic Sciences, of their edible crab resource. The MLS of male Cancer magister is 55: 45–477. 155–165 mm, a value that allows most male crabs to mate at least Anon. 1998. Conservation of fishery resources through technical once before capture, and capture of female crabs is prohibited measures for the protection of juveniles of marine organisms. Council regulation (EC) No 850/98. Consolidated 2004-08-23. (Siddeek et al., 2004). As an alternative for the Skagerrak and the Anon. 2004a. Fiskeriverkets fo¨reskrifter (FIFS 2004:36) om fiske i Kattegat, or in combination with a MLS, there could be a legis- Skagerrak, Kattegatt och O¨ stersjo¨n. National Board of Fisheries, lated change in the size of the present mandatory escape gap to Sweden. 107 pp. avoid capturing undersized crabs. The diameter of the circular Anon. 2004b. Forskrift om endring i forkrift om fangstforbud, gap would need to be increased from its present 75 mm to fredningstid, minstema˚l m.v. ved fangst av hummer, krabbe, 90–92 mm. Such a gap size can be estimated from a length–CW kamstsjatkakrabbe og haneskjell. J-102–2004. National Board of regression (Brown, 1982), assuming that length is a discriminating Fisheries, Norway. character. Additionally, the manipulative experiment with differ- Bennett, D. B. 1995. Factors in the life history of the edible crab ent escape gaps conducted here showed that a 90 mm gap is (Cancer pagurus L.) that influence modelling and management. needed for crabs 135–139 mm CW to escape (Table 4). The catch- ICES Marine Science Symposia, 199: 89–98. ability of ovigerous females in creel fisheries (for crab and lobster) Brown, C. G. 1982. The effect of escape gaps on trap selectivity in the is so low that restriction on landing probably does not need to be United Kingdom crab (Cancer pagurus L.) and lobster (Homarus considered. However, the bycatch of ovigerous female crabs in, for gammarus (L.) fisheries. Journal du Conseil International pour l’Exploration de la Mer, 40: 127–134. example, gillnet fishing for lumpfish or flatfish, which causes high Brown, C. G., and Bennett, D. B 1980. Population and catch structure levels of crab mortality, does need to be assessed. Seasonal closure of the edible crab (Cancer pagurus) in the English Channel. of the crab fishery during peaks in moulting may be necessary to Journal du Conseil International pour l’Exploration de la Mer, 39: decrease handling mortality of crab pre-recruits and recruits, 88–100. particularly if fishing effort burgeons. Campbell, A., and Eagles, M. 1983. Size at maturity and fecundity of The catch potential will be affected along the Skagerrak coast rock crabs, Cancer irroratus, from the Bay of Fundy and south- but to a lesser extent in the Kattegat (Figure 9). Stock assessment western Nova Scotia. Fishery Bulletin US, 81: 357–362. of crustacean fisheries (Smith and Addison, 2003) estimates both Charniaux-Cotton, H., and Payen, G. 1988. Crustacean reproduction. short- and long-term yield benefits from instituting an appropri- In Endocrinology of Selected Invertebrate Types, pp. 279–303. ate MLS, and it also yield other advantages that make the manage- Alan R Liss, New York, USA. ment action acceptable to stakeholders (the professional fishers). Christiansen, M 1969. Decapoda Brachyura. Universitetsforlaget, Length cohort analyses of edible crab on the east coast of England Oslo. 143 pp. have shown long-term gains in yield per recruit and biomass per de Lestang, S., Hall, N. G., and Potter, I. C 2003. Reproductive biology recruit attributable to increases in the MLS (Addison and Bennett, of the blue swimmer crab (Portunus pelagicus, Decapoda: Portunidae) in five bodies of water on the west coast of Australia. 1992). In addition, increasing fishing effort to overcome short- Fishery Bulletin US, 101: 745–757. term losses did not counterbalance the long-term gain to the Defeo, O., and Cardoso, R. S. 2004. Latitudinal patterns in abundance population. Considering stock–recruit relationships and the and life-history traits of the mole crab Emerita brasiliensis on higher economic value of larger crabs may even result in greater South American sandy beaches. Diversity and Distributions, 10: gains than are immediately obvious, but density-dependent effects 89–98. may limit those benefits. Assessments of the effects of an increase Drach, P. 1939. Mue et cycle d’intermue chez les Crustace´sdećapods. in the minimum size at first capture of Dungeness crab Cancer Annales de l’Institut oceánographique Monaco, 19: 103–391. magister in the USA and Canada indicate increases in future Dybern, B. 1983. Tinor fo¨r krabbfiske under hummerns fredningstid. harvest rate (Siddeek et al., 2004), i.e. increases in yield. 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Sexual maturity, larval release and on the size composition of ovigerous females for comparison with reproductive output of two brachyuran crabs from a rocky interti- other maturity characters, and two anonymous referees whose dal area in central Portugal. Invertebrate Reproduction and comments helped improve the manuscript. The study could Development, 42: 21–34. not have been performed without support from the Gaertner, D., and Laloe´, F. 1986. E´ tude biome´trique de la taille a` pre- SUCOZOMA programme and the development project Swedish mie`re maturite´ sexuelle de Geryon maritae Manning et Holthuis, West Coast Crab. 1981 du Seńe´gal. Oceanologica Acta, 9: 479–487. Sexual maturity of Cancer pagurus in the Skagerrak and the Kattegat 327

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Reproductive condition of Dungeness crabs, Cancer magister, at or near log transfer fasilities doi:10.1093/icesjms/fsl039 II

Fisheries Research 84 (2007) 345–357

Movement of adult edible crab (Cancer pagurus L.) at the Swedish West Coast by mark-recapture and acoustic tracking Anette Ungfors a,∗, Hans Hallback¨ b, Per G. Nilsson a a Department of Marine Ecology, TjärnöMarine Biological Laboratory, Göteborg University, S-452 96 Strömstad,Sweden b Institute of Marine Research, National Board of Fisheries, S-453 30 Lysekil, Sweden Received 6 March 2006; received in revised form 10 November 2006; accepted 12 November 2006

Abstract Movements of the edible crab Cancer pagurus were investigated from mark-recaptures in the Skagerrak and Kattegat. Crabs were released in 1968–1973 and in 2003 from six main areas along the Swedish west coast, and from one offshore bank in the Kattegat. Recaptures were reported for up to 7 years after the release. Sex-specific differences in migration were found: females migrated significantly longer distances than males, and higher proportions of males stayed within the area of release (60 and 48% of males versus 28 and 19% of females) were recaptured within 1 km of the release site: initial and recent mark-recapture studies, respectively. The movement direction varied with sampling location, however females tended to move in a net southerly direction. The range of mean rates of movement within the first month were 325–345 m d−1 for females and 202–299 m d−1 for males. Over longer time periods mean rates of movement were significantly lower. There was no significant impact of size class on the distance migrated. Short-term (2 months) movements of nine male edible crabs were studied with acoustic transmitters and active tracking. The movement pattern varied among individuals: some stayed in the same area for weeks whereas some made regular movements every day during the tracking period. The difference in migration pattern of females and males, and the largely southward migration of females is consistent with the hypothesis that the migration is related to reproduction. By moving to the south to release their larvae, females may compensate for larval dispersion in the northbound current along the Swedish west coast. The observed migration pattern indicates advisable management options in Sweden for this commercially fished species: protection of areas with high proportion of egg-bearing females from fishing, especially in the Kattegat. Significantly, local management only on a small spatial scale is not recommended as the resource is seasonally shared, if not the effect on the crab population is monitored. © 2006 Elsevier B.V. All rights reserved.

Keywords: Edible crab; Cancer pagurus; Mark-recapture; Acoustic tracking; Migration; Management

1. Introduction but also on the regional oceanography (e.g. directional currents, topographic gyres and cross shelf currents) and hydrological The dispersal ability of a species is related to that species’ parameters (temperature, salinity). The distance of dispersal dif- population structure (Bohonak, 1999), so that higher dispersal fers among adults according to the life-style: benthic and sessile, ability in general is associated with decreased differentiation benthic and non-sessile, or pelagic. A non-sessile species has the (e.g. measured by genetic distances) among populations. Con- potential to disperse over geographic areas, also as an adult. At sequently, knowledge of the dispersal processes during the entire the extreme, larval dispersal and adult movement can interact life cycle of a species i.e. larval dispersal and the juvenile/adult and result in high dispersal, or counteract and result in rela- life style may give an estimate on the geographic distribution of tively low realised dispersal despite high dispersal potential for a population and the connectivity among populations (Jennings, both larvae and adult. For commercial species knowledge of the 2001; Hellberg et al., 2002). The larval distance of dispersal population structure is important for management reasons. For depends not only on the biology of the species (e.g. larval devel- example, Begg et al. (1999) discuss the importance of identify- opment time, hatching season and larval swimming behaviour), ing the stock structure of a species in order to manage a ﬁshery effectively. Here we describe a study on the migration of a commer- ∗ Corresponding author. Tel.: +46 526 686 88; fax: +46 526 686 07. cial crustacean species with a hypothesised moderate dispersal E-mail address: [email protected] (A. Ungfors). potential. The edible crab Cancer pagurus (L.) has plank-

0165-7836/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2006.11.031 346 A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 totrophic larvae that are pelagic at least for 60 days at temperatures of 15–20 ◦C(Nichols et al., 1982; Thompson et al., 1995). Adults are characterised as mobile and benthic. The distribution of the edible crab on the European Atlantic Coast stretches from the Lofoten Islands, Norway to Portu- gal (Christiansen, 1969). In Sweden edible crab occurs on the west coast in the Skagerrak and Kattegat. The fishery of edible crab in Sweden is small (registered landings in 2004 were 164 tonnes) but has potential to increase as fishermen switch from declining fish stocks. The fishery is open year-round but most professional crab fishermen fish during July–November. A large but un-quantified amount of edible crab is taken by amateur fishermen during the summer months. Both sexes are harvested, but as the price for females is higher, fishermen tend to choose areas were females dominate (higher female frequency in captures, Ungfors, pers. observations). There is no regulated minimum landing size (MLS) but obligatory Ø75 mm gaps in traps and fyke-nets allow the escape of individuals smaller than 110–115 mm CW.The carapace width at size of maturity (CW50) based on gonad development in Swedish waters is 132 mm for females and 117 mm for males (Ungfors, submitted). In this paper we report the study of movement patterns of sub- adult and adult edible crabs on the Swedish west coast. Long and short-range movements of adult edible crab have been studied with different mark-recapture techniques and in different Euro- pean areas; claw-tagging lost during moulting on the North Sea coast of UK (Mistakidis, 1960; Mason, 1962), persistent suture- Fig. 1. On the map are the seven release areas on the Swedish west coast and tagging in the English Channel (Bennett and Brown, 1983), the offshore Kattegat shown. Circles show release areas in the 1968–1973 study and Bay of Biscay (Latrouite and Le Foll, 1989) and east coast of squares show release areas in the 2003 study. The arrow points at the area of England (Edwards, 1979) and ultrasonic transmitters in Scotland Acoustic tracking. (Hall et al., 1991) and Norway (Skajaa et al., 1998). We present previously unpublished data from a tagging study undertaken in the late 1960s and movement data from a recent tagging study crabs and 3135 crabs in Skagerrak and Kattegat, respectively in 2003. The recent study used different mark-recapture areas (Table 1). During the tagging exercise crabs were released on the to the initial study but also used one area in common. Acoustic fishing grounds or occasionally on crab grounds in close vicin- tracking of males was also performed in 2005 to gather infor- ity. The bathymetry of the two basins differs substantially: the mation on short-term movements. We specifically investigate Skagerrak deepens steadily offshore (maximum depth 700 m, sex-specific differences in distance, direction and rate of move- mean depth 210 m (Rodhe, 1996)), while the shallow Katte- ment, and analyse whether migration occurs seasonally, whether gat basin has a maximum depth of 124 m (mean depth 23 m) it is size-dependent. We also investigate the movement pattern of interspersed with shallower 20–30 m offshore Banks (Fonselius, repeatedly recaptured individuals. Movement patterns are com- 1995). In the acoustic tracking study crabs were fished and pared between areas and between studies (i.e. 1968–1973 and released in a small shallow coastal bay (maximum depth 20 m, 2003). The causes of movement, their effect on stock structure, 58◦51N, 11◦08E, Fig. 1) within 1 month (4, 5, 16 and 29 June and their management consequences are discussed. 2005). In this study distances between collection and release locations were less than few hundred meters. 2. Materials and methods 2.2. Tagging and recapture 2.1. Study area Crabs were mainly caught by professional fishermen Between 1968 and 1973 a total of 3749 crabs were tagged although some crabs used in the initial study were sampled and released in three areas along the Swedish Skagerrak coast by Scuba diving. Three marking methods were used in the (Fig. 1, Table 1). Seventy-eight percent of the females and 74% mark-release studies: in the initial study crabs were marked by of the males were released between September and December, a modification of the suture-tagging technique first described the remainder between January and August. The recent mark- by Mistakidis (1959). Numbered plastic discs were posterior release study in 2003 took place at two coastal areas in Skagerrak attached by a braided Terylene thread through two holes pierced and two coastal areas in Kattegat, and at an offshore fishing bank in the carapace epidermal suture. The recent study used two tag- in Kattegat (Fig. 1). The total number of marked crabs was 4975 ging methods: (i) T-bar tags were inserted through a 2 mm hole A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 347

Table 1 The release and recapture number, and average carapace width of edible crabs Cancer pagurus marked in different areas in (a) the 1968–1973 and (b) the 2003 study for females and males, respectively Release location Releases Recaptures Carapace width (mm)

Number of females Number of males Number of females Number of males Mean ± S.D. (females) Mean ± S.D. (males)

(a) 1968–1973 mark-recapture study Fjallbacka¨ 712 732 326 (46%) 199 (27%) 155 ± 17 147 ± 15 Brofjorden 337 140 121 (36%) 22 (16%) 155 ± 15 147 ± 16 Lysekil 1058 770 389 (37%) 193 (25%) 152 ± 16 143 ± 15 Sum 2107 1642 836 (40%) 414 (25%) Total 3749 1250

(b) 2003 mark-recapture study Stromstad¨ 1420 764 111 (7.8%) 38 (5.0%) 139 ± 17 134 ± 22 Fjallbacka¨ 1708 1083 127 (7.4%) 77 (7.1%) 140 ± 17 138 ± 20 Tistlarna 274 119 35 (12.8%) 13 (10.9%) 152 ± 15 143 ± 17 Katt. Inshore 794 365 38 (4.8%) 13 (3.6%) 151 ± 51 140 ± 18 Katt. Offsore 1144 439 156 (13.6%) 80 (18.2%) 168 ± 63 158 ± 18 Sum 5340 2770 467 (8.7%) 221 (8.0%) Total 8110 688

Edible crabs in the range of 95–209 mm carapace width were marked. Releases in 1968–1973 study generally occurred in September–December, while release periods in 2003 were: Stromstad¨ 1–9 September, Fjallbacka¨ 23–28 June and 26–29 August, Tistlarna October–December, Offshore Kattegat 18–19 August, inshore Kattegat 1–2 December. drilled in the epidermal suture. Eight cm long numbered plastic ity of variances was tested using Leveneˇıs test and the data ID-bands hung from these tags and could be readily observed. were log-transformed when necessary. For some data sets, vari- This type was used at the offshore and inshore Kattegat area. ances could not be made homogenous by transformation. For (ii) In the Skagerrak (area Stromstad¨ and Fjallbacka)¨ and the these analyses (mentioned in the text) we show the resulting northern Kattegat (area Tistlarna) black cable ties with yellow p-values, although these should be interpreted with caution. numbered discs tightened around the merus segment of the first Fisher’s LSD were used as post hoc test. The impact of size periopod (claw) were used as a mark. The tagging procedure on total movement distance was statistically analysed with took mainly place aboard the fishing boats direct after capture one-factor ANOVA (four levels, ≤120, 121–140, 141–160 and and crabs were released within 2 h in close vicinity to the capture ≥161 mm CW). For illustration of direction of movements, bear- location. Information about the mark-and recapture project was ing data were grouped into eight directions using 45◦ intervals spread to Nordic fishermen and authorities. (0◦ ± 22.5, etc.) and the pattern shown in spider diagrams. Due For acoustic tracking, nine male edible crabs were marked to uncertainties of exact location of some recaptures (e.g. miss- (dorsally secured with glue on the carapace) with ultrasonic ing details as on which side of a small skerry the recapture transmitters (Sonotronics IBT-96-1; 25 mm × 8 mm, 1.5 g; 21 occurred or in situ estimation of distance to shore, etc.), we Day Life-Time; range 500 m+; 69–77 kHz). During a 2-month include movements of more than 1 km in the directional anal- period (or until the transmitter expired) the crabs were actively yses. In order to assess whether this arbitrary 1 km limit is tracked using a directional Vemco VR 60 and the GPS position too strict and introduces bias we also present direction analy- was taken every, or every second day. The technique allowed for ses with shorter movements from the recent study. Statistical individual identification. analyses of movement direction involved a Goodness of fit test against an expected 1:1:1:1 ratio using the G-statistic (Sokal and ◦ 2.3. Analysis Rohlf, 1995) of directions grouped into four 90 interval (North 316–45◦, East 46–135◦, South 136–225◦, West 226–315◦). To Distance and direction of movement of recaptured crabs were compare movement distance between seasons tagging month calculated in the GIS programme ArcView 3.2 (ESRI inc.) using and recaptures within 30 days were considered. Seasonal move- the extensions Animal movement (USGS-BRD, Alaska Bio- ments and differences in rate of movements based on elapsed logical Science Center) or Path, with distances and Bearings time before recapture (four levels) were analysed with one- 3.2 (Jenness Enterprises, USA). Factorial Analysis of Vari- factor ANOVAs and Fisher’s LSD post hoc test. Recaptures − ance (two-factor ANOVA) was used to compare movements less than 1 km and rates considered unrealistic (>3000 m d 1) (total individual distances) between areas and sexes. For statis- were excluded in the rate analysis. A test of independence using tical analyses, data sets were repeatedly balanced by randomly the G-statistic (Box 17.8 Sokal and Rohlf, 1995) were used to sampling an equal number of crabs from each group. For cal- compare the distribution of directions towards N:E:S:W from culating means and associated measures of uncertainty shown Fjallbacka¨ release area between the periods for comparing recap- in figures and tables, the entire data set was used. Homogene- ture rates. 348 A. Ungfors et al. / Fisheries Research 84 (2007) 345–357

recaptured once (Table 1), and of these 206, 63 and 5 individuals were recaptured two, three and four times, respectively. The recapture frequency of females (40%) was signiﬁcantly higher than the recapture frequency of males (25%) (G-test of independence, G = 5.2, p = 0.023). The last reported recapture from the 1968–1973 study occurred in 1977, 7 years after the crab was marked. In the 2003 study 50% of recaptures were within 1 month, 89% within a year and 10% in the second year (Fig. 2). The recapture rate of females (8.7%) was similar to the recapture rate of males (8.0%) (G-test of independence, G = 0.03, p = 0.86). Repeated recaptures occurred: of the 688 recaptured individuals (Table 1), 48 were recaptured twice and 1 three times.

3.2. Pattern of movement

3.2.1. Distance and direction Females migrated longer distances than males, and in some areas were the frequency of longer movements larger than in others (Table 2, Fig. 3). Females moved on average 6.4–21.7 km and males 1.5–8.8 km (range of area specific means) (Table 3). The frequency of longer movements increased with time before recapture, especially for females (Fig. 4). Female long-range movements (>5 km) were predominately towards north and south from Stromstad,¨ Fjallbacka¨ and inshore Kattegat, towards south from the Brofjorden, Lysekil and Tist- larna and towards east from offshore Kattegat release area (Fig. 5). Movements >20 km were towards south in 78 and Fig. 2. The number of recaptures by days after release. The time after release is divided into twenty-seven 30-day periods, and the number of recaptured crabs 62% of the female migrations from coastal areas, 22 and 33% per interval are shown for (a) the 1968–1973 and (b) 2003 mark-recapture study. were toward north and less than 5% in eastward or west- The number given at the x-axis is the last day in each interval. The regular annual ward direction in the initial (ntotal = 162) and recent (ntotal = 58) increases in recapture rate indicate the Autumn periods. study, respectively. Statistical analyses of direction pattern con- firmed differences between areas and preferred directions within 3. Results areas: The frequency of movements toward the four compass points (N:E:S:W ± 45◦) differed among release areas in the 3.1. Pattern of recapture initial and recent study, for both sexes and movement-ranges (Goodness of fit test; GHeterogeneity, p = 0.0001–0.03). The Most recaptures came within 2 years of release, and the only exception to this pattern was for long-range movements temporal pattern of recoveries showed marked annual peaks of of males in the initial study. The female direction pattern was recaptures in autumn (Fig. 2). In the 1968–1973 study 28% of not uniform toward the four cardinal directions (Goodness of fit all recaptures was recaptured within 1 month, 87% during the test; preplicates < 0.001–0.042) except for short-range data from first year and 12% in the second year. 1250 individuals were Fjallbacka¨ in the recent study (Table 4). In most cases statisti-

Table 2 Distance calculations and statistical analyses (individual total distance) for the 1968–1973 and 2003 mark-release studies 1968–1973 study 2003 study Females Males Females Males

Proportion>1km 72% 40% 81% 52% Mean ± S.D., median, 13.0 km ± 23.2, 2.9 km, 1.9 km ± 4.6, 0.7 km, 11.2 km ± 17.4, 4.0 km, 4.4 km ± 8.3, 1.8 km, q25–q75, max, n 1.2–10.3 km, 228 km, 0.3–2.1 km, 60 km, 1.8–10.8 km, 130 km, 0.7–3.8 km, 59 km, n = 836 n = 414 n = 467 n = 221 ANOVA log-transformed Significant interaction (pinteract = 0.01) in unbalanced but not Significant interaction (pinteract = 0.003) in unbalanced but factors: sex and area; in balanced (8 of 10 random samplings of data not in balanced (10 of 10 random samplings of data pinteract dependent variable: pinteract = 0.065–0.74, n = 22). Sex and area significant 0.081–0.623, n = 13). Sex and area significant (psex < 0.0001 total distance (m) (psex < 0.0001 and parea ≤ 0.043). Heterogenous variance. and parea > 0.0001–0.031, except parea = 0.109 in 1/10 of Fisherˇıs LSD: longer distances for females, Fjallbacka¨ samplings). Heterogenous variance of 8/10 samplings. differ from Brofjorden & Lysekil Fisherˇıs LSD females longer distances, especially Fjallbacka¨ differ from other locations A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 349

Fig. 3. Individual total distance presented as Boxplots (percentiles, median). (a) Females and (b) males in the 1968–1973 study and (c) females and (d) males the 2003 study. Sample size (n) is given. In (a) is the extreme distance value (*) at 228,147 m excluded. cal analyses (Goodness of ﬁt test, preplicates) were not calculated longer distances compared to July, August and Septem- for males due to few replicates (Table 4). An overview of the ber). Males did not show a similar pattern (pmales = 0.249). movements, based on Arcview layouts of all female move- In the 2003 study crabs of both sexes moved longer dis- ments from all the release locations in the 2003 study, is given tances in August compared to June (Fig. 7, one-factor in Fig. 6. ANOVA pFemUnbalanced = 0.004, pFemBalanced = 0.063, n = 8 and pMaleUnbalanced = 0.005, pMaleBalanced = 0.002, n = 4). 3.2.2. Season In the 1968–1973 study females moved longer distances 3.2.3. Size in autumn months than in summer months (Fig. 7, one-factor There was no signiﬁcant difference in total distance between ANOVA pfemales < 0.0001, Fisherˇıs LSD October and November four tested size classes (≤120, 121–140, 141–160 and ≥161 mm

Table 3 Distance calculations per area for (a) the1968–1973 study and (b) the 2003 study Females Males

Mean ± S.D. Median q25–q75 Max n Mean ± S.D. Median q25–q75 Max n (a) 1968–1973 study Fjallbacka¨ 12.6 ± 23.1 2.5 0.8–10.6 137 327 1.5 ± 4.1 0.6 0.1–1.7 36 197 Brofjorden 13.4 ± 20.7 5.9 2.2–11.5 117 120 3.4 ± 5.9 1.4 1.0–2.7 28 22 Lysekil 13.3 ± 24.2 2.8 1.2–10.1 228 389 2.1 ± 5.0 1.1 0.3–2.4 60 193 (b) 2003 study Stromstad¨ 12.6 ± 21.2 5.2 2.3–10.8 130 111 3.2 ± 4.4 1.7 1.0–3.1 18 38 Fjallbacka¨ 11.6 ± 17.7 3.5 0.9–17.2 121 127 4.9 ± 11.4 0.6 0.2–3.3 59 77 Tistlarna 21.7 ± 22.7 7.7 6.0–43.3 71 35 3.2 ± 1.9 3.5 1.1–4.7 6 13 Katt Insh 16.2 ± 17.1 12.1 3.9–18.1 72 38 8.8 ± 11.1 2.6 1.2–14.2 32 13 Katt Offsh 6.4 3.5 1.5–5.6 44 156 3.9 ± 6.0 2.5 1.5–3.8 40 80 350 A. Ungfors et al. / Fisheries Research 84 (2007) 345–357

Fig. 4. The histograms show the distance distribution at different times before recapture. The total number of recaptures per time interval is distributed among ﬁve different distance classes: 0–5, 5–10, 10–50, 50–100 and >100 km. The time intervals are grouped on basis of lapsed months before recapture, from within 1 month to more than 24 months. Female frequency is shown in (a) for the 1968–1973 and (c) for the 2003 mark-recapture study. Male frequency is given in (b) for the 1968–1973 and (d) for the 2003 mark-recapture study. Sample size per time interval (n) is shown on top of each bar.

CW), neither females nor males in the two studies (one-factor ment females and for males within 1 month was signiﬁcantly ANOVA, p > 0.24). higher than movement rates of crabs recaptured after a longer time period (Table 5, one-factor ANOVA log-transformed data, 3.2.4. Rate of movement pfemales < 0.0001 and pmales < 0.0001, Fisherˇıs LSD: females The rate of movement for females and males was grouped 1 month > 2–6 months > 7–12 months ≥ 12 months, males according to elapsed time before recapture. The rate of move- 1 month > 2–6 months = 7–12 months = >12 months) in the

Table 4 Comparison of direction pattern between areas and statistical analyses of direction within an area in the (a) 1968–1973 and (b) 2003 mark-release study Fjallbacka¨ Brofjorden Lysekil

(a) 1968–1973 mark-release study Females 1–5 km 45:30:56:14, p < 0.001 11:5:25:19, p < 0.001 57:96:17:41, p < 0.001 >5 km 71:1:55:0, p < 0.001 3:4:55:2, p < 0.001 32:15:85:7, p < 0.001 Males 1–5 km 16:17:27:9, p = 0.02 4:3:4:4 30:25:9:22, p = 0.012 >5 km 1:0:3:0 0:0:2:1 7:2:6:0

Stromstad¨ Fjallbacka¨ Tistlarna Katt. Inshore Katt. Offshore

(b) 2003 mark-release study Females 0–5 km 24:4:24:3, p 0.001 25:17:23:14, p = 0.25 ns 1:5:0:0 5:0:7:0 7:81:15:17, p 0.001 1–5 km 21:3:23:2, p <0.001 18:9:11:5, p = 0.042 1:5:0:0 5:0:4:0 6:61:14:16, p 0.001 >5 km 27:0:29:0, p 0.001 24:2:22:0, p 0.001 4:0:24:1, p 0.001 13:3:7:3, p = 0.02 3:25:3:5, p 0.001 Males 0–5 km 7:8:14:3, p = 0.047 17:19:14:15, p = 0.83 ns 6:2:2:0 3:2:2:0 5:29:23:7, p = 0.000 1–5 km 5:3:13:1, p = 0.002 6:4:7:5, p = 0.82 ns 3:2:2:0 0:2:2:0 5:25:16:7, p = 0.000 >5 km 4:0:2:0 4:2:6:0 2:2:0:1 1:1:2:2 0:11:1:4

The data is summarised as the number of edible crabs toward each of four directions: North (316–45◦), East (46–135◦), South (136–225◦) and West (226–315◦). Data is statistically analysed with Goodness of fit test: p < 0.05 means a significant difference of the observed distribution compared to an even (25% in each direction) distribution. Analyse not performed if n ≤ 20. ns = non-significant. A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 351

Fig. 5. The movement frequency toward eight different directions for female and male crabs in the 1968–1973 and 2003 mark-recapture study. In (a) are female movements longer than 5 km and in (b) are male movements longer than 5 km summarised. The direction interval is 0◦ ± 22.5◦,45◦ ± 22.5◦,90◦ ± 22.5◦, 135◦ ± 22.5◦, 180◦ ± 22.5◦, 225◦ ± 22.5◦, 270◦ ± 22.5◦, 315◦ ± 22.5◦. Sample size (n) is given for each release area. The scales on the axes differ between 50, 80 and 100%.

1968–1973 and the 2003 study. The maximum rate of move- 3.3. Comparison of movements in time ment of all recaptures were 8377 and 3965 m d−1 for females, and 841 and 1968 m d−1 for males (initial and recent studies, The Fjallbacka¨ release area was used in both studies, and respectively). therefore we were able to compare statistically the distance and 352 A. Ungfors et al. / Fisheries Research 84 (2007) 345–357

Fig. 6. The graph shows the individual female movements from the release areas in the 2003 mark-release study. The central map framed with intervening sections, shows Skagerrak and Kattegat in whole and the four other are magniﬁcations of coastal segments. Unﬁlled circles indicate points of release. direction data. For females, the mean distance (km, ±S.D.) for distances independent of investigational period (two-factor the two periods was 9.5 km ± 19.9 (n = 433) and 10.6 km ± 17.1 ANOVA, psex < 0.0005, n = 82). The distribution of directions (n = 139) and for males 1.2 km ± 3.7 (n = 244) and 4.6 km ± 11.1 (N:E:S:W) was similar between the investigational periods for (n = 82). Statistical analyses showed that females moved longer females and males, both for all movement data combined,

Fig. 7. The average distance (km) in different months of the year from (a) the 1968–1973 and (b) 2003 mark-recapture study for females and males, respectively. Calculations are based on crabs recaptured within 1 month of release. The sample size (n) is shown on top of each bar. Standard error bars are shown. A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 353

Table 5 The mean (±standard deviation and sample size) rate of movement (m d−1) within a speciﬁed time interval from the 1968–1973 and 2003 study, for females and males, respectively 1968–1973 study 2003 study

Females Males Females Males

One month 325 (±469, n = 139) 202 (±184, n = 35) 345 (±302, n = 193) 299 (±304, n = 81) 2–6 months 137 (±175, n = 145) 46 (±31, n = 16) 166 (±175, n = 109) 71 (±75, n = 37) 7–12 months 48 (±69, n = 335) 14 (±23, n = 90) 97 (±107, n = 65) 38 (±47, n = 21) >12 months 49 (±52, n = 124) 9 (±21, n = 51) 53 (±49, n = 55) 27 (±30, n = 18) as well as for only considering movements longer than 1 km Crab 8, released in northern part of the bay stayed there but (G-test of independence, pfemales all = 0.59, pfemales>1km= 0.91, moved between two near-lying stone areas. pmales all = 0.61 and pmales>1km= 0.88). 4. Discussion 3.4. Repeated recaptures in the 1968–1973 study We found that females moved longer distances more fre- For 63 females that were recaptured a second time (move- quently than males, in all the seven locations and in both ments > 1 km), we analysed whether movement continued in the investigational periods. On average females moved 1.8–8.4 same direction or not. Of these, 16 females were recaptured a times farther than males. Movement patterns at the location that third time. Most of the repeated recoveries were made within was common to both studies (Fjallbacka)¨ showed consistency in the same year but some showed movements extending more distance and direction. However, the majority of recaptures of than 1 year. We classified the difference in direction of consecu- both females (89% in 1968–1973 and 92% in 2003) and males ◦ ◦ tive movements into four 90 (±45 ) intervals between first and (>99% in 1968–1973 and 98% in 2003) moved less than 36 km second recapture: 43% of the females moved in the opposite (20 miles). This result is similar to others from inshore in the ◦ direction (difference ± 136–180 ), 32% made further move- English Channel (Bennett and Brown, 1983). Our acoustic track- ◦ ments in same (difference < ±45 ) direction, and the remainder ing of males showed both directed and irregular movements ◦ moved perpendicularly (difference ± 45–135 ) in relation the over thousands of meters indicating that males, like females, first recapture direction. This was significantly different from can show directional movement behaviour. In general however, an expected random 1:2:1 (same: intermediate: opposite) ratio the shorter average distances and more uniform direction pat- (Goodness of fit test, G = 26.7, p < 0.001, n = 63). Of the 12 tern indicate that males were more prone to stay in an area repeated recaptures (between first and second recapture) involv- than were females, and their rather short movements were more ing movements >5 km, 4 continued in a same direction and 7 in like exploratory routes in all directions, probably searching for the opposite direction (G = 81.9, p ≤ 0.001, n = 12). females, new habitats, preys or a response to seasonal temperature changes. Females on the other hand carried out long-range 3.5. Acoustic tracking migrations southwards or northwards along the Skagerrak and Kattegat coast, and eastwards and northwards offshore Katte- The total movements (total distance per individual) over the gat. Mark-recapture studies in other regions have shown that tracked period ranged between 689 and 5440 m (Table 6). The females move more frequently than males (e.g. English Chan- movement behaviour of male crabs varied such that two of the nel (Bennett and Brown, 1983), Bay of Biscay (Latrouite and Le crabs (1 and 3) were more prone to move over the actively tracked Foll, 1989) and east coast of UK (Edwards, 1979)). However the period of 27–45 days (Table 6). Crab 1 moved back and forth frequency of long migrations from the eastern and French side within an area (close to the coastline of a small island) while of the English Channel was higher than we found (Bennett and crab 3 moved consistently south. In fact, a professional fisher- Brown, 1983; Latrouite and Le Foll, 1989). This indicates similar man captured one crab 146 days after the last recorded tracking but regionally influenced movement patterns of C. pagurus over position, during which time the crab had moved approximately its geographical distribution. Movement studies of Cancer mag- 26 km (179 m d−1) south. The individual mean rate of move- ister (Pacific Coast of North America (Jensen and Armstrong, ment over the tracked period was between 28 and 147 m d−1 but 1987)) showed that females were more migratory than males the movement could be as high as 922 m from 1 day to another. in southern British Columbia (Smith and Jamieson, 1991). On Crabs 4, 5 and 9 moved SSW from the release area (which had the other hand, the limited migrations of C. magister in an a relatively soft substratum) to an area with stones and coarser Alaskan deep fiord-type estuary showed that males had larger bottom substrate, and stayed then within these. Crab 2 moved home ranges than females, 3.75 and 0.4 km2, respectively (Stone from its release area central in the bay towards west and stayed and O’Clair, 2001). Home ranges (the largest area covered by all at a shallow depth close to the coastline of a small island. Crab 5 individual positions of recapture or tracking) in our study was moved from the northern part of the bay towards the southwest. many magnitudes larger, particularly for females but was not After a short period of moving from location to location crab 6 calculated due to lack of data points in our mark-recapture data stayed in a small stone area before heading towards southwest. and the short (acoustic) tracking duration for the males. In north- 354 A. Ungfors et al. / Fisheries Research 84 (2007) 345–357

ern California 46% of female C. magister moved < 2 km, and the 124)

± stocks were considered to be “extremely localized” (Diamond and Hankin, 1985). We found 41% of recaptures after 12–24 months, and 27% of recaptures after 2 years, were within 5 km of S.D. 7 1376 21 6 124 (82 ± ± ± ± ± ± the release point (initial study, equivalent ﬁgures for recent study are 27 and 50% but these are based on few recaptures). Conse- Mean quently female C. pagurus could be regarded as highly localized on the Swedish west coast. The male population was even more 22 72

± localized (89 and 64% of recaptures after 12–24 months; 86 33 38 21 26 and 50% after 2 years, within 5 km, initial and recent studies, 9 respectively). There is a risk of misinterpreting a stock as being “localized” 68 28

± with the mark-release method as the crabs may have moved 41 31 extensive distances and back during the period until recapture. 8 Mark-recapture studies that use conventional tagging methods to study movement patterns of marine species have been shown to 37 46 “tell the truth, but not the whole truth” (Bolle et al., 2005). On the ± 41 31 Swedish west coast, trawling has been allowed closer and closer 7 to the coastline during the 20th Century but the trawling bound- ary was moved out to 3–4 nautical miles in 2004 (Anon., 2006). 96 50 From the mid-1980s Norway lobster (Nephrops norvegicus) has ± ) is calculated from the individual mean rate over the tracking period. 45 33 been captured in creels, mainly inshore of the trawling bound- − 1 6 ary and in the northern area of Swedish Skagerrak coast (Anon., 2006). Static gears (pots) for lobster (Homarus gammarus) and 71 67 edible crab have been used commercially since beginning of ± 29 14 20th Century and are extensively in use, generally aggregated

5 closer to the shore but also offshore on the banks in Kattegat. These ﬁsheries are all capable of ﬁshing crabs and for that rea-

97 76 son no serious limitations or spatial differences in fishing effort ± 27 24 exist on the Swedish west coast. However, the temporal pattern 760 419 400 566 694 153 772 228 467 553 353 178 146 135 169 168 197 170 160 1681 1698 2537 1706 2340of 689 recoveries 2373 is most probably influenced by fishing practices as the frequency of recaptures peaks at approximately 30, 300 and 690 days, in both investigational periods. The Swedish monthly 111) 77 landings of edible crab are highest in August to November (2005 ± log-book data, National Board of Fisheries) due to high meat yields (Ungfors et al., 1999) and high catchability (Bennett, 79 (106

± 1995). In addition, the annual opening of the Swedish ﬁshery 45 (191) 30 (31) for lobster (with by-catches of edible crab) in late September 34

E) within 1 month starting the 4 June 2005. The crabs were tracked for 33–45 days every 1–2 days. Movement data including recaptures of crab 1 results in large numbers of lobster traps and a corresponding

08 increase in the chance of reports from recaptured crabs during ◦ 47 92

± this period. N, 11 33 20 304 787 (26,169) 357 447 169 153 Several hypothesis to explain migration patterns for Can- 1360 3909 (30,078) 51 ◦ cer spp. have been presented: inshore migration for moulting, mating (females and males) and spawning and offshore hatch-

216) 53 ing migration (Diamond and Hankin, 1985), migrations toward ± exposed area for spawning (Smith and Jamieson, 1991), mating migration or pre-hatching emigration to avoid osmotic stress

218 (143 (Orensanz and Gallucci, 1988)ofC. magister, feeding migra- ± tion in C. novaezelandiae (Chatterton and Williams, 1994) and 44 (77) 129

Crab 12 female migrations related to moulting and mating in C. pagurus at the north east coast of Scotland and England (Mason, 1962; Edwards, 1979). The extensive westerly or south-westerly ) 147 ) 922

− 1 migrations in the English channel (Bennett and Brown, 1983; − 1 Latrouite and Le Foll, 1989) are against the prevailing eastern- directed Channel current (Dahlgaard, 1995; Guegueniat et al., 1995). Bennett and Brown (1983) point out that this may be an Max distance (m)Total days 956 Tracking occasions 29 (30) Mean rate (m d Table 6 Data summary from acoustic tracking of nine male edible crabs Total movement (m) 5440 (6108) The crabs were released in a Swedish coastal bay (58 CW (mm) and 3 in the commercial fishery, 1 and 5 months, respectively, after tracking, is shown in parentheses. Gross movement (m month Max rate (m d offshore migration towards grounds suitable for spawning and/or A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 355 counteracting larval drift, and therefore having consequences for ing period, Ungfors, 2006) and for that reason there is no need the replenishment of eastern stocks in the Channel. They could for a compensatory migration every year. Ovigerous females are not find evidence for return movements of the adults, but did find rarely captured in baited creels and are observed to congregate in some easterly movements from the inshore (westerly located) deep water (Howard, 1982) indicating that females are inactive release areas. Stress of repeated capture and handling may during embryogenesis. The spawning period in Swedish waters impact crab behaviour, and technical mistakes (e.g. incorrect is in late November to January (Ungfors, pers. observations) reporting from fishermen, or wrong recording of crab number by and larvae can be found from April to October (Thorson, 1946). the fishery biologists) are possible. However, in our study, over The most probable period for migration related to reproduction 40% of the repeated recaptures were towards opposite direction in Swedish waters is therefore the autumn, before the winter between first and second recapture, which could be interpreted as spawning and inactive period, after the hatching and regaining return movements. This is an important finding as understanding feeding summer period. This is also what we found: for females of biology and implementation of proper management need not the average distance of movement was higher during autumn only to be aware of the one-way migration but also of possible than summer months. However, none of our long-range migrat- returns, which theoretically re-establish the stock state. ing females were in the ovigerous state at recapture (or release). The prevailing surface current along the Swedish west coast This controversy between theory of migration and the evidence is northward (Rodhe, 1996). A northward dispersal of pelagic is probable more due to the fact that collection and recapture larvae could be the underlying reason for the observation that were by pots, and that ovigerous females are captured in low adult females predominantly migrate toward the south when frequency in these gears. In addition to the use of pots and low distances over 20 km are considered. Dispersal of crab larvae catchability of ovigerous females, the time for recapture and for 2 months by a one-directional current of 0.20 m s−1 mean ovigerous state was not synchronised: most of the recoveries velocity (Rodhe, 1996) move the larvae more than 1000 km were in autumns but crabs are ovigerous state in winter-spring. downstream of hatching location. This distance is certainly a Our data suggest that there were no impact of crab size and substantial overestimation of the true dispersal as the direction distance of movement, which is not what we would expect if the of currents may change on daily basis and larval swimming hypothesis that female movements are of reproductive origin. behaviour (not least vertical migration (Harding and Nichols, Size-independency in migration pattern has also been found in 1987; Park and Shirley, 2005)) will impact the realised dis- C. magister (Diamond and Hankin, 1985). In our study the pro- persal distance. However, this simple calculation may indicate portion of small marked females and males was low: only 2% the need for a evolved behaviour, such as the upstream migra- of the females and males were smaller than 120 mm and none tion of females prior hatching or larval swimming behaviour was smaller than 100 mm carapace width. Based on gonad stud- (Shanks and Brink, 2005), to guarantee continued recruitment ies (Ungfors, 2006) the main part of the studied crabs could along the Swedish coast. Eaton et al. (2003) challenge the for- be regarded as sexual mature and the risk of an immediate merly accepted wisdom of a northward movement of females large-scale loss of externally secured tags was therefore not over- along the east coast of England and Scotland that results in south- whelming. While externally secured tags have a lifetime of a ward transport of crab larvae i.e. recruitment to the main fishery couple of years at most, persistent tags may last for longer peri- from the north. Instead the main fishery seem to be on a separate, ods and recaptures after longer periods are possible. A higher self-sustaining population, which may provide adult recruitment frequency of sub-adults may result in a difference in distance to the north of adult crabs. The relatively high percentage of with size. migrations towards north in release areas Stromstad,¨ Fjallbacka¨ The average rate of movement in our study decreased with and inshore Kattegat could be explained either as return move- increasing time elapsed since release, indicating either that crabs ments of females not spawning that year, adult recruitment to had periods of resting during the migrations, or that some indi- the north or regional differences in environment e.g. the water viduals were migrating back to the release areas. Another cause current. The baroclinic northward coastal current (the Baltic cur- for the low rate of movement after longer periods may be that rent) is more pronounced in Skagerrak than in Kattegat due to the individuals have fulfilled their movement in a shorter time (1) the Kattegat-Skagerrak front forcing this low-saline water and were no longer moving. Depending on the time of tagging to contract along the Swedish coast, (2) as a result of the basic and release, rates of movement could be higher with time as the cyclonic current around the Skagerrak and (3) the often strong probability for migratory behaviour is increasing. For example westerly currents towards the Swedish coast from north Jutland if the releases occurred in early spring the rate of movement (Gustafsson and Stigebrandt, 1996). This stronger northward would be small the first month but increasing after longer peri- current around the border between Skagerrak and Kattegat could ods (autumn movement). In both studies most releases were explain the higher frequency of southward movement in the mid in the autumn or late summer and consequently longer periods Skagerrak and northern Kattegat compared to more southern or increased “the risk” of including the coldwater inactive winter- northern coastal release areas. spring season. The average rate of movement within 1 month The relative high share of female recaptures that do not show was around 300 m d−1 for females and 200 m d−1 for males, signs of long migrations may be explained by their natural life which is consistent with rates from offshore release points in the cycle: females are not ovigerous every year after sexual maturity English Channel (Bennett and Brown, 1983) and for C. magister in Swedish waters (about 10–20% of large-sized 134–170 mm in British Columbia (Smith and Jamieson, 1991). For recaptures CW females have their gonads in a “resting” stage in the spawn- between 7 and 12 months migration rates were around 50 m d−1 356 A. Ungfors et al. / Fisheries Research 84 (2007) 345–357

(females) and 14 m d−1 (males) comparable with slow inshore with the 450 km range of the Kattegat and Skagerrak west coast. migrations in the English Channel and with C. magister weekly The proportion of individuals that migrated between Skager- migrations in an Alaskan estuary (Stone and O’Clair, 2001). rak and Kattegat (in either direction) was low but nonetheless Some recaptures show extraordinarily high rates of over 8377 m present, and this probably represents an important component in 1 day. The validity of these data can be questioned but these of gene flow between the two basins. Fisheries targeting oviger- high rates have been reported for the English Channel (Bennett ous adult females during autumn in the Kattegat (Ungfors, pers. and Brown, 1983; Latrouite and Le Foll, 1989). The mean rate of observations) can have seriously negative effects on the fish- acoustically tracked males was 28–147 m d−1 (72md−1 in aver- ery resource along the whole coast if these females function as age), which indicates sizeable variation in migration behaviour a source population. In order to combine a fishery on females even within a short time period. with developed ovaries (the preferred crab product in Sweden), while still maintaining a sufficient larval supply to the north, different management actions can aid in preventing recruitment 4.1. Management consequences over-fishing (Hilborn and Walters, 1992). One among the many options for management would be to implement seasonal clo- Movement patterns of populations obtained from mark- sures or a marine protected area (MPA) on the spawning grounds recapture studies are limited in space and time, which make it in the Kattegat (to protect spawning females) or the implementa- difficult to draw conclusions about population structure. In our tion of protected spawning areas regularly distributed along the study we have movement data from seven different locations Kattegat and Skagerrak coast in combination with catch quotas within a limited area (Skagerrak and Kattegat) spanning more in the basins to guarantee a sufficient migratory proportion of than 30 years. Within a restricted area of kilometres there is no females. Local management only a small spatial scale (hundreds doubt that the shown migration pattern improve the mating pos- of km) is not recommended as the resource is seasonally shared sibilities and mating success. Harder to speculate about is the i.e. Skagerrak and Kattegat should most probably be considered effect of this migration on the population structure. Waples and as one management unit unless genetic markers show the oppo- Gaggiotti (2006) found population differentiation at migration site. However, as it is difficult to say how the movements found in rates up to 0.1–0.2 (the fraction of immigrants in a popula- our study (some long-range movements of females but also evi- tion). In Sweden captures of new-moulted soft crabs occurs in dence of highly localized stocks) would affect connectivity and July–October, which allows moulting, mating and subsequent population independency learning by doing i.e. adaptive man- sperm delivery to occur either before or after movement. As agement (Walters and Green, 1997; Sainsbury et al., 2000) using the moulting period starts during the summer period when as different suitable management actions on relatively small spatial shown in our study, movement rates were lower, sperm deliv- scale in combination with population monitoring and assess- ery may take place before movement, and the mixing of genes ment might be the best management option, and would lead to between crabs from different locations is reduced compared to an increased knowledge of the population dynamics of the crabs. if the mating occurs after movement. This speculation assumes that females are the migratory sex, return movements are a rule Acknowledgements and males are stationary i.e. “immigrants” in an area are of low frequency. The data underlying this manuscript could not have been The genetic population structure studied by genetic mark- compiled without all the fishermen along the Swedish coast ers is the result of long-term mixing processes so studies on who have been cooperating and reporting recaptures, or without differentiation in genetic markers indirectly may indicate the field assistance of Christin Appelqvist and Helena Sundstrom.¨ dispersal (gene flow) of larvae and adults among geographical Many thanks for practical help during the acoustic study to Sven- areas (Bohonak, 1999). However, we are not aware of any pub- Gunnar Lunneryd, Magnus Wahlberg, and all course participants lished data on the genetic structure of C. pagurus in any of its of the Marine Bioacoustics course (June 2005) at TMBL and to distribution area. Despite the prevailing paradigm that pelagic Marie-Laure Begout´ Anras and Marie-Laure Acolas for acoustic larvae confer dispersal (e.g. Hellberg, 1996; Todd et al., 1998; instruments and instructions. We are grateful to Jon Haven- Uthicke et al., 2001) there is evidence for genetic differentia- hand for grammar improvement of the manuscript. We thank the tion in species with pelagic larvae (e.g. for American lobster SUCOZOMA programme, the project Swedish west coast crab, Homarus americanus (Tracey et al., 1975), spider crabs (Weber the Institute of Marine Research, Orvar and Gertrud Nybelin et al., 2000) and sea urchins (Moberg and Burton, 2000)). An Fund for Fishery Biology Research, and Sonotronics for fund- analysis of the genetic variation along the Swedish west coast is ing of these studies. Methodologies undertaken in the studies therefore necessary to complement the results from this mark- comply with the current laws of Sweden. recapture study, to draw conclusions on mixing processes at the population level. The connectivity of populations has profound implications References for the management of these populations. In our study there is Anon., 2006. Effekterna pa˚ utflyttad tralgr˚ ans¨ pa˚ fisk och bottenfauna. Analys evidence that some individuals are highly mobile (females) but av okad¨ anvandning¨ av passiva redskap innanfor¨ tralgr˚ ansen¨ samt de also that a high portion may be resident. Crabs in this investiga- ekonomiska konsekvenserna for¨ naringen.¨ Fiskeriverket/National Board of tion dispersed over distances up to 228 km. This can be compared Fisheries. A. Ungfors et al. / Fisheries Research 84 (2007) 345–357 357

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ICES CM Shellfish Committee No. 88. 219.

III

Lack of spatial genetic variation in the edible crab (Cancer pagurus) in the Kattegat-Skagerrak area

1Ungfors, A., 2McKeown, N.J., 2Shaw, P. and 1Andre, C.

1Department of Marine Ecology-Tjärnö, University of Gothenburg, SE-452 96 Strömstad, Sweden 2School of Biological Sciences, Royal Holloway University of London, United Kingdom

Corresponding author: Anette Ungfors, [email protected], +46 526 686 88

1 1 Abstract The stock structure of the edible crab Cancer pagurus in Kattegat and Skagerrak was investigated using eight microsatellite DNA loci. Samples were collected twice at Grove Bank (N57°) in Kattegat and at Lunneviken (N59°) in Skagerrak, 4-6 years in between. In addition, one sample collected at Midsund (N62°) in the Norwegian Sea was included as an outgroup. The genetic differentiation among samples, estimated as global FST=0.002, is significant (p=0.03) when the statistical test was based on allele frequencies but not when based on genotype frequencies. Moreover, all single-locus and pair-wise FST values were non- significant using both allelic and genotypic tests. Analysis of molecular variance, AMOVA, did not reveal any differentiation between spatial (Kattegat vs. Skagerrak) or temporal groups of samples (2001-2002 vs. 2006-2007). A statistical power analysis suggests that using the same number of loci, sample sizes, and allele frequencies as in this study, we would have a power of >90 % to detect stock differences of the same magnitude as recorded in the present study. The processes behind the low spatial and temporal genetic structure might be a high gene flow in the area due to adult migration and larval dispersal or alternatively, historical gene flow persisting among recently founded large populations. Local management of the edible crab fishery can be considered and implemented whereby stakeholders take a precautionary approach such as implementing size restrictions and not fishing below a certain local biomass.

Keywords: Genetic stock structure, microsatellite DNA, genetic differentiation, FST, gene flow, edible crab

2 2 Introduction A prerequisite for resource management of commercially exploited fish and shellfish species is to define how the resource is partitioned, spatially (geographically) and temporally, i.e. to identify stock units. As for species and population concepts there is no universally accepted definition of what constitutes a stock and there has been a shift towards an adaptive holistic approach admitting the use and need for several purposes (Begg&Waldman 1999; Carvalho&Hauser 1999; Waples&Gaggiotti 2006; Abaunza et al. 2008). All attempts of stock definitions struggle in optimizing a balance on precision and generality, and common words in the definitions are “self-sustaining”, “integrity/sharing”, “spatial/area” and “temporal/time” (Cadrin et al. 2005). In contrary to the species or population concept, there is an underlying meaning of management in the stock definition. The need of conservation of biodiversity or genetic variation within endangered species has resulted in another debated concept of similar nature: evolutionary significant unit (ESU) (reviewed in Fraser&Bernatchez 2001). However, a fundamental difference between stock management and ESU is the aim of maximizing yield of the former unit versus a more life-sustaining aim in an evolutionary perspective of the latter. Different methods to investigate the stock unit have been suggested , which all have their strengths and weaknesses and often reflects the definition chosen by the investigator. The advantage of using a holistic approach is that one of the techniques may detect stock structure where others fail to do so. For example, morphologic or phenotypic characters for stock identification can be biased by environmental modulation so that separate stocks may be indistinguishable due to similar selection effects (Chaceon quinquedens in Gulf of Mexico vs. New England Weinberg et al. 2003) while at the other end of the spectrum directional selection may lead to false estimates of stock heterogeneity (Clupea harengus e.g. in Kinsey et al. 1994).

Genetic markers are powerful tools for describing population/stock structure (Utter 1991 ; Carvalho&Pitcher 1995). A major of population genetics to fisheries management has been to define the concept of ‘stock’ in an evolutionary meaningful way, and to promote the use of this concept in management (Ihssen et al. 1981; Allendorf et al. 1987; Carvahlo&Hauser 1994). The extent of gene flow among populations, mediated by the forces of genetic drift and mutation, determine patterns of variation at selectively neutral genetic loci. Over short time scales the effect of mutation is expected to be negligible with genetic population structure being the product of opposing forces of gene flow and genetic drift. While gene flow is expected to promote genetic homogeneity, populations that are not exchanging genes are expected to acquire differences in frequencies of genetic variants over time by genetic drift. Therefore, by characterising the distribution of genetic variation, population substructuring can be detected and the degree of connectivity among populations estimated (Nesbo et al. 2000; Ruzzante et al. 2000; Hutchinson et al. 2001). From a management point of view this connectivity is often interpreted as a proxy for likelihood of replenishment, or more specifically, if individuals are removed to what extent will replenishment occur by migration (Waples 1998). In this way the ‘genetic’ stock concept focuses on the degree of isolation among stocks.

In general, marine species are expected to show weak population structure over large geographic areas due to fewer barriers, compared to land, and high dispersal ability via larval drift and/or adult movements (Ward et al. 1994). However, intra-specific genetic analyses of commercial decapods have revealed complex patterns of genetic differentiation at various geographical scales. For example, mtDNA restriction fragment length polymorphism (RFLP)

3 3 analysis of European lobster Homarus gammarus revealed distinct genetic clusters and an overall FST estimate of 0.078 among 44 samples from its European distribution range (Triantafyllidis et al. 2005). Similarly, Norway lobster, Nephrops norvegicus, revealed significant differentiation (FST 0.013-0.018) among samples from the North Sea, Irish Sea, Portugal and the Mediterranean, but with no isolation by distance effect or partitioning associated with the Atlantic-Mediterranean division (Stamatis et al. 2004 (allozymes); Stamatis et al. 2006 (mtDNA RFLP)). Studies of decapod species have found genetic variation over relatively short distances like 40, 142, and 225 km (Weber et al. 2000; Weber&Levy 2000; Jorstad et al. 2004). Also, enhanced settling of larvae within 0-6 m of parents, despite a 1-2 week larval dispersal period, have been reported indicating that dispersal potential may not be realised (Knowlton&Keller 1986). Thus, the genetic structure of marine species is determined by the complex interaction of several factors including adult mating and pre-spawning behaviour, larval development time and behaviour, oceanography and its seasonal and annual variation, and must be empirically examined to inform management.

The edible crab Cancer pagurus is distributed in the eastern Atlantic Ocean from the northern part of Norway to north-western part of Africa (Christiansen 1969). The total landings in 2004 were 46 280 tonnes and mainly originate from around the British Isles including UK, Ireland and France. Though, northern areas like Norway have had an increase in landings lately (FAO 2004). Tagging studies from the English Channel (Bennett&Brown 1983), Bay of Biscay (Latrouite&Le Foll 1989), North Sea Coast of United Kingdom (Edwards 1979), and Skagerrak and Kattegat (Ungfors et al. 2007) reveal that female edible crabs have the ability to move long distances over 100´s of kilometres. Laboratory rearing of larvae shows developmental times of at least 50-80 days in 15-20°C (total days in zoea stage I-IV, Nichols et al. 1982), and field surveys indicates that the larvae are pelagic for 2-3 months as this is the time between density peaks of zoea I and megalopae, respectively (Eaton et al. 2003). The fecundity is high, ranging from 0.5 to 2.9 million of eggs female-1 in the mature size range of a female, the larger female the more eggs (Edwards 1979; Ungfors 2007). The size at sexual maturation has been studied in different areas (Edwards 1979; Brown&Bennett 1980; Tallack 2002; Ungfors 2007). In general, females start mating at relatively small sizes at carapace width (CW) ~110 mm but their gonads are not maturing until after one more moult at ~130 mm CW. Contradictory, gonadal development and allometric growth of chela in males show higher consistency between physiological and functional maturity, at 110-120 mm CW.

The aim of this study was to investigate the spatial genetic stock structure of the edible crab in Kattegat and Skagerrak and to examine the temporal consistency of this structure; a sample from the Norwegian Sea was included as an outgroup. This is the first study of genetic population structure of edible crab in this area. The edible crab has a high potential for dispersal during the pelagic larval stage and a mobile benthic life-style during its adult stage. Genetic variation was analysed in 348 individuals captured at three different locations and two occasions using eight microsatellite DNA loci. The outcome of the study is discussed in a management perspective.

Materials and methods Sampling of individuals was performed at three different geographic locations and during different years in order to study the genetic variation on both a geographic and temporal scale.

4 4 Seventy individuals were sampled on each occasion (table 1). The sampling of crabs in Kattegat was performed in August 2001 and June 2007 at an offshore bank, Groves bank (N57°06, E11°31). Samples from Skagerrak were obtained in September 2002 and September 2006 at Lunneviken, a coastal location close to the Swedish-Norwegian border (N59°03, E11°10) (table 1, figure 1). A third location, a coastal location in the Norwegian Sea of mid Norway called Midsund (N62°40, E06°40), was sampled in December 2004. This third location was used as an outgroup.

Genomic DNA was isolated from the claw or the periopod muscle cells using the VIOGENE DNA EXTRACTION KIT (protocol Blood and Tissue Genomic Mini). Eight microsatellite DNA loci (table 2) were amplified with PCR (Eppendorf Mastercycler Gradient) using primers described in McKeown and Shaw (2008) with modified primer annealing temperatures (TA) (Cpag-5D8 TA = 54ºC, Cpag-6C4 TA = 55ºC, Cpag-3A2 TA = 55/52ºC, Cpag-3D7 TA = 54C, Cpag-1B9 TA = 51ºC, Cpag-2A5-2 TA = 58ºC, Cpag-4 TA = 55°C and Cpag-15 TA = 55°C; 30-33 cycles of 1 min 95ºC, 1 min TA and 1 min 72ºC except for Cpag- 3A2 where 10 cycles of 55ºC and 25 cycles of 52ºC was used). Individual locus PCRs incorporated a forward primer labelled with a CY5 tag permitting visualisation on an ALF II express automatic sequencer (Amersham Pharmacia Biotech). Identification of alleles was performed by the use of software ALFwin Fragment Analyser 1.02. To ensure accurate sizing of alleles a suite of size markers specific to each locus (two sizemarkers (ALF expressTM SizerTM 50-500, Amersham Bioscience) external to the allele spread and two size markers within the allele size range (van Oppen et al. 1997)) were run simultaneously (within the same lane) at each amplification. Two control individuals were run across all gels to ensure consistency among runs. Six of the loci (Cpag-5D8 to Cpag-2A5-2) were analysed at TMBL but loci Capg-4 and Cpag-15 genotyped at the School of Biological Sciences, Royal Holloway University of London following similar protocols.

Overall amplification success was 97.7 %. The allele sizes were checked for typing errors with Microsatellite toolkit (Excel add-in, Park 2001) and for potential null alleles using Micro-checker (Van Oosterhout et al. 2004). Genepop on the Web (Raymond&Rousset 1995) was used to calculate for each locus/sample combination the expected heterozygosity (He, Nei 1987) and FIS, and to test for deviations from Hardy-Weinberg equilibrium (HWE). Population structure was quantified using FST (Weir&Cockerham 1984) calculated in GENEPOP. The null hypotheses of FST=0 was tested using both allelic (genic) and genotypic data in GENEPOP. Significance levels were adjusted for multiple tests using Bonferroni correction (Rice 1989). Analyses of molecular variance (AMOVA) (ARLEQUIN, Excoffier et al. 2005) was used to analyse the genetic differentiation due to temporal and spatial groupings: the two samples in Kattegat (GR01, GR07) and the two samples in Skagerrak (LU01, LU06) were grouped either by location (Kattegat vs. Skagerrak) or by time (2001- 2002 vs. 2006-2007).

The statistical power of the markers and sample sizes employed in this study to detect a user- inferred level of population structure (FST) was assessed using the simulation approach in POW-SIM (Ryman&Palm 2006). Five populations with effective population size Ne is allowed to drift for t generations. The expected genetic differentiation FST is calculated by the t Nei (1987) formula FST=1-(1-1/2Ne) , and we simulated a range of FST values. We used Ne of 1000 and 10000 based on earlier estimates of Ne in marine species being three to four magnitudes smaller (Turner et al. 2002; Turner et al. 2006) than census size (Ungfors et al. in

5 5 prep). After t generations a subsample of 70 individuals was taken from each of the five samples, whereafter a FST was calculated. This was repeated for 1000 or 10000 runs. The proportion of statistically significant overall FST outcomes (p<0.05) estimates the power.

Results Micro-checker indicated possible null allele frequencies in the sample from Grove Bank 2001 at locus Cpag-4, and in the sample from Lunneviken 2006 at loci Cpag-5D8 and Cpag-3A2, at 7, 5 and 7-11 % respectively. Allele and genotype frequencies for those loci were adjusted, and original as well as adjusted genotypes were used for calculations of FST for population comparisons. Locus Cpag-4 showed indications of null alleles of low frequency 2.5-5 % in the samples from Lunneviken 2006 and Norway but frequencies were not adjusted.

Out of the 40 comparisons of locus-specific FIS-value, six indicated significant deviation from HWE, and of these two remained significant after Bonferroni correction for multiple comparisons, p=0.05/40=0.00125 (table 3, ***).

The overall genetic differentiation among the samples, global FST = 0.0019. Using genotypic data this estimate was not different from zero (p=0.27), whereas an analysis based on allele frequencies (genic data) indicated an overall structure (p=0.03). This pattern was consistent for all eight individual microsatellite DNA loci, with individual locus FST values ranging between -0.0049 and 0.0088 (table 4). The pair-wise population comparisons revealed no difference in allele frequencies between the five samples; pair-wise FST’s ranged from -0.0008 and 0.0038 (table 5, figure 2). Analyses based on genotype frequencies adjusted for null alleles were similar for overall FST (FST 0.0020, p=0.25), locus-specific population comparisons (FST ranged between -0.0048 and 0.0088, p>0.05) and pair-wise comparisons (FST ranged between -0.0008-0.0040, p>0.05).

The results from the AMOVA indicated neither spatial (Kattegat vs. Skagerrak) (table 6a) nor temporal structure (years 2001-2002 vs. years 2006-2007) (table 6b). However, the AMOVA indicated some difference between samples within the different groupings, in accordance with the genic analysis above (tables 5a,b).

The statistical power, the probability of rejecting the null hypothesis (H0) when it is false, with our sampling design, is > 93 % for a FST of 0.002 (table 7). An expected FST of zero estimates to 0.04-0.05, indicating expected levels of type I error.

Discussion The spatial and temporal genetic differentiation of edible crab is low within 1300 kilometres of waterway distance in the investigated area. This conclusion is supported by i) low global multilocus FST of 0.002 and non-significant single locus FSTs using allele frequencies, ii) non- significant global FST, single locus FST and pair-wise comparisons using genotype frequencyies, (iii) no genetic differentiation among groups in AMOVA and (iv) that statistical power analysis suggested > 93 % power for our sampling design to detect an overall genetic

6 6 differentiation of FST 0.002. Altogether, these results suggest that the genetic variation over a 1300 km water distance, from the basin of Kattegat at 57°N to the Norwegian Sea 62°N is very weak. The reason for this weak structure is discussed below.

Firstly, the lack of spatial genetic differentiation can be explained by a high gene flow over large areas. Female edible crabs are capable to move 100´s of kilometres and the pelagic larvae can disperse over long distances. A hypothesis explaining the pattern and cause of migration of females states that migration is directed towards the prevailing surface current to compensate for larval dispersal (Bennett&Brown 1983). This migration pattern opposite to current direction is valid for some areas, but not for all. Mark-recapture experiments in Kattegat and Skagerrak (Ungfors et al. 2007) demonstrated a large fraction of long southerly directed migrations of females from some coastal locations, thus against the coastal northward surface current, but also long migrations both northward and southward from other locations. There is a lack of knowledge concerning return movement or natal homing behaviour for the edible crab, which is described for other species in connection with spawning (Vannini&Cannicci 1995; Thorrold et al. 2001; Hauser et al. 2006). But there are some observations indicating return movements the edible crab (Robinson et al. 2003; Ungfors et al. 2007), which could explain the northward migrations according to the hypothesis. If the above hypothesis is true, this could result in local genetic populations as the larval dispersal is compensating for the adult migration. Though, the results in this study indicate that adult migratory behaviour vs. oceanographic currents does not genetically structure the population in this area, undermining the above compensating hypothesis. Adult and larval drift seem to cause high gene flow, diminishing genetic variation over a large area.

Secondly, the low genetic differentiation among the individuals within the studied geographic area may reflect historical gene flow persisting among recently founded large populations. The Pleistocene ice ages (1.8 Mya-10 kyr years ago) and particular the last glacial maximum (LGM) 21 kyr years ago have shown to impact the spatial pattern of genetic differentiation of invertebrate species (Macoma balthica Atlantic assemblages, Luttikhuizen et al. 2003) and marine algae (Fucus serratus, Coyer et al. 2003). Northern Europe has repeatedly been covered by ice to a varyingly degree during Pleistocene: the British and the Scandinavian ice sheets, respectively, covered land and extended out to the shelf edge (~200-400 m) during glacial periods from at least 0.5 Mya to LGM. The ice sheets were possible confluent 28-22 14C ka BP (LGM) and ice covered central and northern North Sea regions which otherwise seem to be ice free (Sejrup et al. 2005). The south-western ice limit of the British ice sheet is not fully agreed upon, but the Celtic Sea was partially covered. The modern marine circulation system in Skagerrak was essentially established at about 8 kyr ago when the eastern North Sea coastlines had attained present appearance (Gyllencreutz et al. 2006). The edible crab distributed in Kattegat, Skagerrak and mid Norway at present could, rather than from these areas formerly covered by ice, have been re-colonised from area(s) south of British ice sheet e.g. English channel – Bay of Biscay or possible from a refuge in the North Sea. In this case, the time that has past is likely un-sufficient for genetic differentiation based on genetic drift. This especially counts for a large population which edible crab has had the potential to be (high density, high fecundity), as opposed to a small population where bottlenecks and stochasticity can change the allele frequencies over time to a larger extent. As for the edible crab, lack of migration-drift equilibrium due to recent re-colonisation is also hypothesized to explain the the low genetic differentiation and and absence of geographical pattern of genetic variation in the the European lobster (Triantafyllidis et al. 2005) and the genetic structure of Norway lobster (Stamatis et al. 2004). Areas of possible survival for cod,

7 7 Gadus morhua, populations during LGM have been analysed by environmental modelling. This revealed potential suitable habitats off Atlantic Europe down to at least northern Spain and off eastern North America and Iceland, but only scattered potential habitats around Greenland (Bigg et al. 2007). This is consistent with analysis of genetic data for this species, indicating a long time of population divergence between Europe-Iceland-North America but shorter for Greenland populations in relation to Iceland-Europe (Bigg et al. 2007 and references there in).

A third alternative that may explain the lack of significant genetic differentiation is Type II error: that we have missed the genetic signal for a genetic differentiation due to too few sampled individuals, too few loci or not so variable loci. The sample size of 70 individuals and the use of 8 microsatellite loci is fully comparable with other recent population genetic studies (Jorstad et al. 2004; Laikre et al. 2005a). The allele numbers per locus are variable to hypervariable, varying from 4 to 34 alleles (table 2). Also, the frequencies of alleles within a locus was a mixture of relatively uniform to skewed frequencies (figure 2). Differences in power to detect genetic differentiation, particular at low FST values, have been shown between statistical methods, number of samples and populations, and allele frequency distribution (Ryman et al. 2006). The power analysis performed in this study showed that the analysis had a high power, > 90%, to detect differences between stocks at FST 0.002 (global value in this study), using the same number of loci and sample size, and the allele frequencies as in this study. This strengthens our findings of lack of significant genetic differentiation among the sampled groups.

An assumption of the statistical FST analysis is random sampling so that every individual in the population should have an equal chance of being sampled. However, sampling biological populations is as Waples (1998) underlines typically constrained in time and space. In our study we sampled location Grove Bank and Lunneviken twice with 4-6 years in between (1 generation) to be able to exclude that some e.g. seasonal biological behaviour impacted the outcome. No genetic differentiation was seen between temporal or spatial groups, or in pair- wise FST analyses. However, as the AMOVAs among samples within locations/occasions indicate, there was some differentiation between the samples. This can possibly be explained by temporal instability signalling sweepstakes (Hedgecock 1994) i.e. a temporal change in genetic composition because of small effective population size and random genetic drift. The edible crab is highly fecund and randomly a few of the females may succeed in reproduction whereas other not which cause temporal instability in population allele frequencies.

In general, marine genetic population studies show a relatively low level of genetic differentiation. Studies of decapod species with similar biology as edible crab show upon the complex situation where biology, but also marker, geographical scale, environment and historical events play a role for the conclusions on stock structure. A genetic population study of the hairy edible crab C. setosus, distributed along the 2500 km Chilean coast, found non- significant differentiation by the use of AFLP analysis (Gomez-Uchida et al. 2003). This could possibly be caused by the lack of barriers and effective mixing by northward Peru currents and southward Peru-Chile counter-currents. However, a genetic differentiation (FST 0.026) was shown in the C. setosus based on allozymes. Though this result was not considered reliable since only two allozyme loci were polymorphic and environmental selection could impact the allele frequencies. Despite high genetic diversity within samples, the northern shrimp Pandalus borealis in North-eastern Atlantic group into three main

8 8 clusters partly explained by the retention of larvae within coastal fjords (allozymes, Drengstig et al. 2000; RAPD, Martinez et al. 2006). In a large-scale study the coastal shrimp Crangon crangon groups into three geographical regions with some differentiation within a region (Weetman et al. 2007). Also, a genetic study on a smaller scale within United Kingdom revealed a distinct population of C. crangon from north-eastern UK (Beaumont&Croucher 2006). Clustering of H. gammarus throughout its distribution from Greece to Norway (FST = 0.078) have been shown, but this was explained by regional reduced diversity rather than unique haplotypes (mtDNA) (Triantafyllidis et al. 2005). The genetic pattern of the blue crab Callinectes sapidus on the eastern United States indicate a overall structure, FST (0.04), but with no apparent geographic pattern except for a decrease in haplotype diversity with increasing latitude indicating a historic period of sudden expansion (McMillen-Jackson&Bert 2004). Populations of swimming crab C. danae in southern Brazil differentiate between estuaries only 250 km apart and the investigated populations cluster into two groups separated with at least 550 km. The sampling strategy has a large impact on the study of stock structure, as distinct populations may be extensively mixed during e.g. feeding migrations and thus not identifiable as samples may comprise individuals from multiple populations (Ruzzante et al. 2006). Nesbo et al. (2000) reported elevate populations structure for the Atlantic mackerel (Scomber scombrus) when sampling at spawning periods compared to at other times. In conclusion, unique genetic structures exist for decapod species all around the world and the cause (s) of the pattern differs.

On an evolutionary time frame of thousands or millions of years the investigated area in this study can be looked upon as one genetically based stock unit. However, as only a few effective migrants between sampled locations generation-1 are needed to overcome the effects of genetic drift establishing homogenous allele frequencies (Wright 1931), this stock unit can be questioned on an ecologically time frame of decades. Many studies of marine species have shown significant genetic differences, which could lead the author to recommend the use of multi-stock management. Waples (1998) high-light three other possible outcomes that can occur if H0 (no differences) is rejected, in addition to a correct conclusion. The most important possible outcome to emphasise is that given enough data, significant differences can be expected to occur routinely when comparing geographic samples due to some departures from panmixia. This difference between samples might not be biological meaningful (Hedrick 1999). Therefore the management recommendation of a commercial species after 1) non- significant FST, as in this study, of one single stock unit, or after 2) significant FST of few- several stock units, is not straightforward.

Management In Sweden and internationally, suggestions are raised and research programs are financed for investigations on the potential for local management e.g. the Swedish programme SUCOZOMA Sustainable Coastal Zone Management. Laikre et al (2005b) discuss three types of genetic population structures in relation to fishes in the Baltic Sea, namely distinct, continuous and no differentiation. They conclude that local over harvest, or even extinction of populations with no differentiation, may not have a serious effect on total genetic variation in comparison with the two other genetic population structures, as long as the effective population size is large enough to resist the effect of genetic drift. However, ecological impacts could be serious. Therefore, local management of the edible crab can be considered and implemented whereby stakeholders take a precautionary approach such as implementing size restrictions and not fishing below a certain local biomass. However, local over harvest

9 9 does not severely impact the total genetic pool, as long as no extensive fishery exists on all local management areas and as long as corridors for genetic connectivity between them prevails. Kattegat and Skagerrak landings of edible crab are taken by Swedish, Danish and Norwegian fishermen, and today different regulations are used within these areas; different MLS are legislated along the Norwegian coast (Anon 2004b) but no MLS is in use in Swedish (Anon 2004a) or Danish waters within these areas (Anon. 1998). If exploitation rate increases in the basins, international negotiations on catch or effort limits can be necessary.

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14 14

TABLES

Table 1. Site and date of sampling, sex (no. of females:males) and size distribution (sex-specific carapace width (CW); mean, standard deviation and interval) in the five samples of edible crab Cancer pagurus. Locality Grove Bank Grove Bank Lunneviken Lunneviken West Norway GR01 GR07 LU02 LU06 NO04 Major Kattegat Kattegat Skagerrak Skagerrak Northern sampling area North Sea Sampling site N57.06.21 E11.30.73 N59.03.50 E11.10.00 N62.40.33 (mm.dd.ss) E06.39.77 Date of 2001, 26th of 2007, 4th of July 2002, 27th of 2006, 2004, 4th of Sampling September August September- December October Sample size 70 70 70 70 69 Female:Male 66:4 52:18 51:19 63:7 34:35 CW (mm) F 162±11, 138-186 168±14, 131-193 152±16,122-183 154±17,78-185 152±11,131-180 M 154±17, 131-172 172±12, 160-207 168±16,126-187 146±13,127-167 154±18,122-197

Table 2. Number of alleles, frequencies of most common allele (average for 5 samples) and allele size ranges (bp) per loci.

Locus Number Freq. of Allele size of alleles most range common allele Cpag-5D8 34 0.20 154-265 Cpag-6C4 8 0.38 166-194 Cpag-3A2 4 0.52 255-264 Cpag-1B9 16 0.66 222-286 Cpag-3D7 8 0.45 169-217 Cpag-2A5-2 8 0.54 153-174 Cpag-4 31 0.76 202-295 Cpag-15 8 0.12 124-145 total 117 0.45 124-295

15 15 Table 3. Expected heterozygosity, He, and deviation and exact test from Hardy-Weinberg expectancy (HWE), FIS, for single loci, in the five samples of edible crab. The number of private alleles per sample are also given. Locus Sample GR01 GR07 LU02 LU06 NO05 He FIS He FIS He FIS He FIS He FIS Cpag5D8 0.91 -0.02 0.91 -0.00 0.88 0.08 0.90 0.11 0.90 0.04 Cpag6C4 0.69 0.03 0.72 -0.03 0.73 0.02 0.70 -0.17 0.69 -0.00 Cpag3A2 0.57 -0.04 0.57 -0.11 0.58 -0.20 0.58 0.21 0.59 -0.04 Cpag1B9 0.48 -0.02 0.56 0.06 0.59 0.05 0.45 0.07 0.50 -0.03 Cpag3D7 0.64 -0.11 0.68 -0.10 0.66 0.03 0.69 0.15 0.65 0.10 Cpag2A5-2 0.52 0.12 0.49 -0.05 0.51 -0.04 0.53 -0.20 0.57 -0.19 Cpag-4 0.95 0.14*** 0.94 0.03 0.94 -0.01 0.94 0.08*** 0.95 0.10 Cpag-15 0.44 0.07 0.46 0.01 0.44 -0.01 0.35 0.06 0.33 -0.04 No. of private 3 2 1 3 6 alleles Bold FIS values differ significantly from zero (p<0.05; no correction). Two of the six significant FIS remained significant after the Bonferroni correction (p=0.05/40=0.00125) (***locus Cpag-4 in GR01 and LU06).

Table 4. Overall genetic differentiation among edible crab samples, FST, for single loci and all eight loci combined. Statistical significance is calculated using both genotypic and genic data.

Locus FST P genotypic P genic Cpag-5D8 0.0021 0.220 0.061 Cpag-6C4 0.0023 0.151 0.117 Cpag-3A2 -0.0049 0.994 0.994 Cpag-1B9 0.0088 0.164 0.0498 Cpag-3D7 0.0057 0.459 0.347 Cpag-2A5-2 -0.0018 0.700 0.668 Cpag-4 0.0005 0.290 0.215 Cpag-15 0.0031 0.153 0.042 All loci 0.0019 0.272 0.0297* Significance level P<0.05, and adjusted for Bonferroni correction =0.05/8=0.00625.

16 16 Table 5. Pair-wise FST. a) FST (below diagonal) and p-value (above diagonal, genotype frequencies=genotypic test) for pair-wise comparison between the five samples for all eight loci. b) FST (below diagonal) and p-value (above diagonal, allele frequencies=genic test) for pair-wise comparison between the five samples for all eight loci.

Table 5a.

GR01 GR07 LU02 LU06 NO GR01 - 0.43 0.64 0.08 0.49

GR07 0.0033 - 0.76 0.36 0.13 LU02 0.0019 -0.0008 - 0.13 0.31 LU06 0.0012 0.0031 0.0038 - 0.82 NO 0.0010 0.0026 0.0035 0.0005 -

No significant pair-wise comparisons.

Table 5b.

GR01 GR07 LU02 LU06 NO

GR01 - 0.28 0.38 0.063 0.25

GR07 0.0033 - 0.57 0.13 0.051 LU02 0.0019 -0.0008 - 0.016 0.16 LU06 0.0012 0.0031 0.0038 - 0.50 NO 0.0010 0.0026 0.0035 0.0005 -

Significant level after Bonferroni correction =0.05/10=0.005. No significant pair-wise comparisons after adjusted significance level.

17 17 Table 6. AMOVA result. a. Grouping according to location i.e. Kattegat (GR01 and GR07) vs. Skagerrak (LU02 and LU06). b. Grouping according to occasion i.e. in 2001-2002 (GR01 and LU02) vs. 2006-2007 (GR07 and LU06). The Norwegian sample is not included in theses analyses.

Table 6a.

Source of variation d.f. Sum of Variance Percentage of p-value squares components variation Among locations 1 1.770 -0.0054 -0.26 1.000 Among samples 2 6.607 0.0084 0.40 0.024* within locations Within populations 556 1176.021 2.115 99.86 0.051 Total 559 1184.398 2.118 100

Table 6b. Source of variation d.f. Sum of Variance Percentage of p-value squares components variation Among occasions 1 2.359 -0.0023 -0.11 0.686 Among samples 2 6.018 0.0064 0.30 0.021* within occasions Within populations 556 1176.021 2.1151 99.81 0.068 Total 559 1184.398 2.1192 100

18 18 Table 7. Analysis of statistical power of rejecting the null hypothesis H0 of no differentiation when false. The simulations of different expected FST below, at and above the observed overall FST, from t effective population size and generations (FST=1-(1-1/2Ne) (Nei 1987), and the resulting proportion of significant Chi and Fisher tests after 1000 or 10000 runs, namely the power. The proportion of significant test with no simulated genetic drift (t=0) estimates , indicating (expected) type I error.

Expected Average Chi-test Fisher´s Ne Generations (t) runs FST FST test 0.0010 0.0010 0.57 0.54 1000 2 1000 0.0010 0.0010 0.54 0.52 10000 20 1000 0.0020 0.0020 0.96 0.94 1000 4 1000 0.0020 0.0020 0.95 0.93 10000 40 1000 0.0020 0.0020 0.96 0.94 1000 4 10000 0.0020 0.0020 0.96 0.94 10000 40 10000 0.0050 0.0050 1.00 1.00 1000 10 1000 0.0050 0.0050 1.00 1.00 10000 100 1000 0.0000 0.0000 0.040 0.050 1000 0 1000 0.0000 0.0000 0.040 0.048 10000 0 1000

FIGURES

Figure 1. Genetic population study of edible crab Cancer pagurus. The map show the geographical distribution of the three sampling locations: Grove bank (GR) in Kattegat, Lunneviken (LU) in Skagerrak and Midsund (NO) in the Northern North Sea. Grove bank and Lunneviken were sampled twice in 2001 and 2007, and in 2002 and 2006, respectively.

19 19

Figure 2. Allele frequencies of all eight loci and five samples (GR01, GR07, LU02, LU06, and NO).

20 20 IV

Effective fishing area, crab density and stock abundance of the edible crab (Cancer pagurus) in Swedish waters using mark-recapture experiment and GIS modelling

1Ungfors, A., 1Nilsson, P.G. and 2Sundström, H

1Department of Marine Ecology-Tjärnö, University of Gothenburg, 452 96, Strömstad, Sweden 2Department of Systems Ecology, Stockholm University, Sweden

Correspondence author: +46 526 686 88, [email protected]

Keywords: mark-recapture, bait attraction, effective fishing area, edible crab density, stock abundance, suitable habitat

Abstract Here we present an estimate of the total abundance of adult crabs (Cancer pagurus) on the Swedish west coast, based on a combination of experimental fisheries to get catch per unit effort data and effective fishing area, and GIS modelling of available habitat. Fishery-related data, e.g. catch per unit effort (CPUE), is often used as a substitute for direct density assessments for estimating trends in stock size. In order to translate CPUE data from static gear (e.g. baited crab pots) to stock biomass or number, it is necessary to know the catchability coefficient q also defined as effective fishing area, i.e. the area over which all individuals of the target species are caught in one pot assuming that the pot is capturing 100% of the crabs within this area. In a mark-recapture experiment we estimated the effective fishing area around crab pots targeting edible crabs (Cancer pagurus). Crabs were caught and marked at 5 locations in the Kosterfjord, Swedish Skagerrak coast in September 2003. Crabs were then released at 5 distances (10-160 m) in four directions from a baited pot. The number of marked crabs caught in the baited pot was then followed daily for 5 consecutive days. The current speed and direction close to bottom during the experimental period was measured daily with a drift buoy. In total, 1635 crabs were marked, and 45 crabs were recaptured (2.8%). The effective fishing area q was estimated to 2293 ± 1137 m2 (mean ± 95% confidence interval), corresponding to a circle with a radius of 26.6 ± 6.3 m. In a separate experimental fishery in the Fjällbacka archipelago located approximately 35 km south of the Kosterfjord during June and August 2003, we estimated catch per unit effort at two depths strata (15-18 m and 25-30m) at 7 locations. CPUE did not differ significantly between seasons or depths, but differed significantly among locations. Using the effective fishing areas estimated around a string of seven pots, we calculated an average density of 0.0038 ± 0.0015 crabs/m2. Using GIS data on depth and sediment characteristics of Skagerrak and Kattegatt we calculated the area of suitable crab habitats along the Swedish West coast. We defined a suitable crab habitat to be between 10 and 40 meters water depth, and with a bottom consisting of bedrock, stone, gravel or sand. The area of suitable crab habitat was estimated to 4142 km2, which combined with density estimates from Fjällbacka would indicate that the catchable population of crabs on the Swedish west coast would be approximately 1.6x107 ± 6.3x106 crabs.

2 Introduction Knowing the abundance or density of a commercial species of fish or crustaceans is important for management, e.g. for estimating the potential of a fishery in the early stages of development, for modelling the effect of different management regimes, and for evaluating the efficiency of existing management. Direct visual observation on abundance in marine habitat is often more effort demanding compared to observations of terrestrial species because of the 3D and low transparency of the oceans. However, diver observations (Miller 1989; Wolff&Soto 1992; Karlsson&Christiansen 1996), underwater filming using remotely operated vehicles (ROV) (Stevens 2003; Busby et al. 2005) or cameras (UWTV) (Hughes&Atkinson 1997; Tuck et al. 1997; Morello et al. 2007) on sledges are in use. Mark- recapture methods are indirect alternative for stock estimation where the recapture of marked individuals and e.g. the Jolly-Seber method have allowed for stock size estimation in an open population of e.g. Cancer pagurus (Bell et al. 2003) and Carcinus maenas (Munch-Petersen et al. 1982). For many fisheries, data from the commercial fishery, commonly catch per unit effort (CPUE), is the only means available to estimate density. However, CPUE data must be used with caution, as many factors besides the abundance of the target species may influence CPUE, e.g. soak-time, gear saturation, changes in gear efficiency, changes in fishing grounds, the skills of the fishermen, and many other causes (Bennett&Brown 1979; Miller 1990; Hilborn&Walters 1992; Miller&Addison 1995; Shelton 2001). If these factors are taken into account, CPUE may be used as an index to assess if changes in the abundance of the targets species occur. However, if CPUE is also to be used as an index of absolute abundance (e.g. number of individuals per m2), then some kind of translation of CPUE data must be applied. The general conversion factor is the catchability coefficient q such as

CPUE=qN where N is the stock size, and q defined as the fraction of the stock captured by a unit of fishing effort (Ricker 1975). The catchability coefficient has also been termed as the effective fishing area (reviewed in Miller 1990). The effective area is the area from where the captured crab came from assuming that 100 % of the individuals are captured, and should not be confused with the wider attraction area (Himmelman 1988; McQuinn et al. 1988) i.e. the maximum area from where individuals could be attracted. The area of effective fishing or attraction can be estimated by several methods, e.g. by direct behavioural studies (Sainte-Marie&Hargrave 1987; Skajaa et al. 1998), using traps in a string investigating overlapping areas or not (Bell et al. 2001; Aedo&Arancibia 2003) or use of independent estimation of abundance (diving) and CPUE (Miller 1989). An alternative approach is to use mark-recapture methods (Bell et al. 2003). A way of using mark-recapture to estimate effective fishing and attraction area, is to release marked animals at different distances from a trap, and then recording the number of recaptured animals during a certain time period, or using one release point and many traps at several distances around this point (Acosta&Perry 2000). In this study we estimate the catchability coefficient q for edible crab (Cancer pagurus) in Skagerrak as the effective fishing area using the mark-recapture strategy (release at different distances and directions from a central crab pot) and using a model previously used to extimate insect densities using baited traps (Byers et al. 1989; Turchin&Odendaal 1996; Östrand&Anderbrant 2003). A graph of the distance (r) from the trap on the x-axis and the 3

3 proportion of recaptured individuals (P(r)) on the y-axis can then be used to estimate the maximum distance that an animal can reach the trap in the time interval, which is obtained by the intercept with the x-axis. This measure is called the attraction range (rs), and it is dependent on the time that the trap is employed. The effective fishing area q is the area around the trap from which all animals originate if the trap catches all the animals within the area and no animals outside this area. The effective fishing area q can be obtained from the formula

where rs and P(r) is obtained from the graph described above. This is in a sense an artificial concept, as no trap probably works this way, but it is a convenient way of calculating density from the trap catch, by the formula

Density= Catch/q where the catch can be taken e.g. from logbook or research survey CPUE data.

Material and methods

Estimation of effective fishing area The experimental fishery was made during September 2003 on 5 locations in the Kosterfjord on the Swedish Skagerrak coast (table 1). Crabs were initially caught on each location with 60 pots of the type used in the commercial crab fishery in Sweden. The crabs caught were measured and marked with a numbered plastic band on each claw (figure 1). Two baited pots (figure 1) were then placed on each location, and crabs from that location were released at 5 different distances from these two pots (10, 20, 40, 80 and 160 m) in the four cardinal directions (north, west, south and east). On each location, the number of crabs released was increased with distance from the central pots (figure 2). The total number of crabs released differed slightly among localities and was dependent on the number of crabs caught during the initial fishery (table 1). The central pots were first checked for crabs caught after 24 hours, and then every 24 hours for 4 consecutive days. The number marked and unmarked crabs of each sex were recorded. The attraction range and effective fishing area were calculated as described by (Östrand&Anderbrant 2003). In short, if the distance of release from the central collecting pots is plotted on the x-axis against the proportion of crabs caught on the y-axis, the intercept of a fitted line with the x-axis is a measure of the sampling range rs (the maximum distance from where a crab can reach the pot during the fishing period) i.e. attraction range. The effective fishing area q (the area from where the crabs are attracted if the pot was 100% effective at catching crabs) is calculated from the probability function of recapture from distances 0-rs from the central collecting pots.

Figure 1. Cable-ties were used as marks (left), central pot (mid) and drift buoy (right). To test if the current direction would influence the area of attraction, the current close to the seafloor was measured with a drift bouy (figure 1), first when the crabs were released and later each time the pots were checked for marked crabs. The drift bouy was allowed to drift for 30 minutes on each occasion, and the position at the start and end of the period was recorded. The average speed and direction was then calculated in the GIS software ArcGIS 9.0 (Esri Inc.).

Figure 2. Experimental design. Marked edible crabs were released at five different distances from two central pots (black dots). The number of released crabs increased from the short distance to the maximum: 10 m 4-6 crabs, 20 m 5-15 crabs, 40 m 10-35 crabs, 80 m 10-35 and 160 m 15-63 crabs. This was repeated on 5 locations.

Estimate of CPUE CPUE was estimated in a trial fishery during 6 days in June (23d – 28th) and 5 days in August (25th – 29th) 2003, in the Fjällbacka- Väderöarna area on the Swedish west coast (11°03 N 58°36 E; 11°10`N 58°36E: 11°05 N 58°33 E, 11°12 N 58°35 E) in a chartered 9 m (29.5 feet) commercial crab fishing vessel. The experimental fishing was designed to resemble methods, seasons and locations used by commercial fishermen. Fishing gear were common pots (70x45x45 cm) with metal skeleton and nylon mesh, with 75 mm escape gaps. Seven traps, 15 m apart, were tied together with rope, forming so-called strings .14 strings were distributed at seven locations: three locations in the inner part of archipelago (Småsvinningarna, Kyrkogårdsön and Skottarna), three locations in the outer part (Knappen, Hamnerö and Ärholmen), and one location on the ground Stora Ryggen in the fjord separating the inner and outer archipelago. At each location two strings were used, one at shallow depth (15-18 m) and one deeper (25-30 m), since these are depths commonly used by commercial fishermen during these seasons. Traps were hauled and put back on the same place every day during the

5 experiment, except the first day in each session when traps only were set. Weather conditions also forced us to cancel the fishery during one day in each fishing session: 24th June and 27th August. Thus we got both 24 and 48 hours soak-times. The catch in 48 hours soak-times were converted to 24 h by the conversion factor 1.1, estimated from a data set (Hallbäck, H unpublished). Data was taken on sex, size (carapace width (mm)), shell condition (indicating time since moulting, on a scale from one to five, where one is newly moulted and five is long time since moulting), lost claws, location, depth, position of trap in string, soak time and recaptures. All crabs were returned to water at the site of capture.

Extrapolating density estimates to the Swedish west coast. We estimated the available crab habitat by a modelling approach in the GIS software ArcGIS 9.0 (Esri Inc.). Data on depth and sediment characteristics with a spatial resolution of 600 m-7 km (depending on the actual area) for the entire Kattegat and the eastern part of the Skagerrak was obtained from the BALANCE project (BALANCE 2007). From this, areas with suitable depths (10-40 m and sediment characteristics bedrock and other hard substrates, gravel and sand) were plotted, and their area was calculated. The area included in the analysis was based on sites reported in logbooks from crab fishermen during the years 2004-2007 (data obtained from the Swedish National Board of Fisheries). The area of suitable crab habitats was calculated in the GIS, and this was then combined with the estimates of effective fishing area per pot and CPUE (described above) to form an estimate of the available abundance of crabs.

Results

Effective fishing area In total, 1635 crabs were marked on the five locations, and 45 crabs were recaptured (2.8%). The number of marked and recaptured crabs on each location is given in table 1. Table 1: Number of crabs measured and recaptured on the 5 locations.

Location Position Crabs Crabs marked recaptured Arsklåvet 58°50,090; 296 7 11°07,42 N Rossöflaket 58°51,054; 197 5 11°07,293 Kalvörännan 58°50,30; 350 9 11°01 40 N Grötholmen 58°53,609; 557 18 11°06,057 Ramsöflaket 58°50,500; 234 6 11°04,30

The proportion of recaptures decreased with distance for all 5 locations (an example from one locality is given in figure 3), although the pattern is less clear on some localities beacause of the low number of recaptures. 6

Figure 3. The proportion of recaptured edible crab from increasing distance from the central pots. Data from location N Grötholmen.

We could not find that the current pattern significantly affected the attraction of pots. The proportion of recaptured crabs did not differ significantly among the four directions for any of the locations (2 goodness of fit-test against a null hypothesis of equal number recaptures in all directions ), except for Ramsöflaket where more than expected recaptures came from the east. However, as the prominent current direction was toward the south or towards the north, the relatively high capture rate on crabs released east of the pots in not easily explained by the currents.

The attraction range rs varied between 159 and 343 meters for the five locations (table 2).

Table 2. Attraction range rs, effective fishing area, and radius of effective fishing area, and estimated density on the 5 locations. Mean± 95% confidence interval, n=5.

Location Sampling Effective fishing area q Radius of q 2 range rs (m) (m ) (m) Arsklåvet 214 2077 26

N Rossöflaket 159 1426 21

Kalvörännan 343 3828 35

N Grötholmen 171 1846 24

Ramsöflaket 250 2290 27

Average estimate 227 ± 92 2293 ± 1137 26 ± 6.5

Despite the variation among locations in estimates shown in table 2, the regression lines of proportion recaptured vs. distance were not significantly different among locations (Analysis of Covariance, Interaction F4,94=1.23, P=0.305, Location F4,89=0.77, P=0.548). Therefore, we may average the results from all 5 locations to get an overall estimate of the attraction range of 227± 92. The effective sampling area varied between 1426 and 3828 m2, corresponding to radii of between 21 and 35 m. The average estimate of radius of attraction was 26 ± 6.5 m.

Catch per unit effort The catch per unit effort varied between 2 and 119 crabs caught per string and 24 hours. The catches at different depths or seasons did not differ significantly (factorial ANOVA), but there were significant differences both among Fishing days and Locations (p=0.0001 and p=0.0006 respectively), and in the interaction among them (Season*Location p=0.0009; Location*Fishing day p=0.03; Depth*Fishing day*Locations p=0.001). The other interactions were not significant, and are hence less important in explaining the variations in catches. Fishing success does hence depend on location and day, but also on season. There are better catches at shallow water in June than in August and conversely higher catches at deep than shallow water in August. Catches are also significantly higher (p=0.0047) at the inner locations (Småsvinningarna, Skottarna and Kyrkogårdsön) in June than in August. Additionally there are daily differences on each location on what depth gives highest catches (Table 3).

Table 3. CPUE per string averaged over all fishing occasions at different locations, seasons and depths (mean ± 95% confidence interval, n= 4 for June, n= 5 for August).

Hamnerö Kyrkog/ Skottarna Småsvinn St. St. & L. Ärholme Lyngö . Ryggen Knappen n June 9.5±9.4 54.0±15.5 53.5±20.9 30.5±15.5 41.7±15.5 24.0±11.8 14.9± 9.1 15-18 m 25-30 m 16.7±7.2 46.1±24.7 46.9±15.5 8.6± 7.1 53.6±35.5 22.3±12.4 17.7± 7.5 August 12.4±9.5 7.8±3.3 12.2±9.5 26.7± 4.6 21.4±19.6 16.4±17.3 8.6± 4.9 15-18 m 25-30 m 23.1±4.5 22.9±16.7 28.9 ±17.0 13.1± 7.7 27.6±15.4 40.5±25.5 20.4±15.3

The overall average of all fishing days, depths and occasions and taking the 7 localities as replicates is then 26.6 ± 9.4 (mean ± 95% confidence interval) crabs caught per string and 24 hours. As each string consisted of 7 pots, with partly overlapping effective fishing areas, we calculate a combined effective fishing area for a string to 7022 ± 1366 m2 (using the average

8 effective fishing radius of 26 ± 6.3 m from table 2 above). The average density of crabs at the 7 locations is then CPUE/effective fishing area = 26.6/7022 =0.0038 ± 0.0015 crabs/m2. Extrapolating density estimates to the Swedish west coast. The area of suitable crab habitat (as defined by hard and sandy substrates between 10 and 40 meters) along the Swedish west coast is calculated to 4142 km2 (figure 4). Using the density value of 0.0038 ± 0.0015 crabs/m2 obtained from the experimental fishery in Fjällbacka, we get an overall density estimate of crabs in the parts of the Skagerrak-Kattegat area visited by Swedish fishermen of 1.6x107 ± 6.3x106 crabs.

Figure 4. Suitable crab habitat (greyish) defined as 10-40 m depth with sediment characteristics bedrock, gravel and sand. The landing positions in 2004-2007 of crab gears are shown.

Discussion Miller (1990) reviewed findings on effective fishing area and concluded that catchability coefficients on shallow bottoms have been in tens and hundreds of square metres whereas values from deep flat habitats have been in thousands of square metres. Our finding on effective fishing area do more closely resemble those of deep-water species such as the snow crab Chionoecetes opilio with a q of 2470-5290 m2 (Miller 1975), and the red crab Geryon maritae with q of 2160 m2 (Melville-Smith 1986). However, Bell et. al. (2003) estimated the effective area fished per trap of Cancer pagurus to 5851-10301 m2 (95% confidence interval) comparable or even larger than our estimate 1426-3828 m2. Earlier finding for the shallow-living species C. irroratus is 276 m2 (80 mm CW, average q for kelp and barren habitat), whereas q was smaller for smaller individuals (Miller 1989). Aedo and Arancibia (2003) estimated q to 577 m2 for the Chilean lemon crab C. porteri. Miller (1989) also estimated the catchability coefficient for American lobster Homarus americanus to 373 m2 (70-89 mm CL), where q also was smaller for smaller individuals. The q estimates for edible

9 crab in our study is for crabs larger > 75 mm CW similar to the size range in Bell et.al. (2003, > 70 mm CW). Bell et. al. (2003) found a density of 0.0021 crab m-2 for edible crab on the East coast of UK, comparable to our density estimation of 0.0038±0.0015 crab m-2. The density of deep-water stone crab Paralomis formosa (Lithodidae) was in average 0.008 individuals m-2 using photographs and prediction on effective area of bait odour plume (Collins et al. 2002). Cancer polydon in the Northern Chile is more dense, 0.15 individuals m-2 estimated from night dives (Wolff&Soto 1992). Previous experiments in Norway by Skajaa et. al. (1998) based on behavioural data collected by telemetric tracking of crabs estimated an attraction distance of 28 m, significantly lower than the pooled value of 198 m (rs) we found in our mark-recapture experiment. Our estimation of attraction area is dependent of time, so time difference (we used five days for estimation and Skajaa (1998) used one night and instant attraction) may have cause the difference. However, our effective fishing radius is close to Skajaa (1998) attraction distance. We used two pots for attraction to avoid gear saturation effects (Miller 1990) e.g. to avoid that attracted crabs did not enter because of inter-specific avoidance of aggressive large males. This might have impacted the effective fishing area most probably overestimated the area resulting in an underestimation of the density. Our estimate of q is based on a recapture rate of 2.8 % as 45 of the 1635 marked crabs were recaptured. This low recaptured rate could have had an impact on the results. Many biological characters of the edible crab may impact the catchablity in fishing gear e.g. feeding intention, moulting, spawning, hatching and migration (Bennett 1995). As these characters are time-dependent the time of the season is an important driver for catchability. We estimated the catchability coefficient in September i.e. during the main fishing period. Three components contribute to the overall uncertainty in the estimate of total stock size: effective fishing area (q), CPUE (from the experimental fishery in Fjällbacka), and the GIS analysis of habitat area. To reduce the combined uncertainty and thus improve the estimate of total abundance, trial fisheries should ideally be repeated in other areas along the coast, to assess the geographical variation. A more detailed analysis of fishermens logbooks may help, but the current varying level of detail in the logbooks makes this complicated. The uncertainty of the GIS estimate of habitats is more complex: this is dependent on a number of different datasets, each with its own uncertainty. However, as detailed mapping of marine habitats progresses, these types of data sets will become more reliable. A last important part is of course to make investigations of the actual habitats preferences of crabs. More directed investigations using fishery-independent data (e.g. divers, video or ROV) of the habitat preferences of different size-categories of crabs will be necessary to make estimates of total abundance more reliable. Acknowledgements We are grateful towards the fishermen Lars-Åke Olsson, Långasjö and Morgan Axelsson, Strömstad for all collaboration during the experimental fishings. Many thanks to Christin Appelqvist for assistance during the fishing experiments, markings and for being an exemplary skipper on Doris. And to Hans Hallbäck for the crab capture data used for soak- time conversion.

10 References

Acosta CA, Perry SA. 2000. Effective sampling area: A quantitative method for sampling crayfish populations in freshwater marshes. Crustaceana 73, 425-431. Aedo G, Arancibia H. 2003. Estimating attraction areas and effective fishing areas for Chilean lemon crab (Cancer porteri) using traps. Fisheries Research 60, 267-272. BALANCE. 2007. Zyad Al-Hamdani and Johnny Reker (eds.). 2007. Towards marine landscapes in the Baltic Sea. BALANCE interim report #10. Available at http://balance-eu.org/ . ISBN: 978-87-7871-203-5. Bell M, Addison JT, Bannister C. 2001. Estimating trapping areas from trap-catch data for lobsters and crabs. Mar. Freshwater Res. 52, 1233-1242. Bell M, Eaton D, Bannister R, Addison JT. 2003. A mark-recapture approach to estimating population density from continuous trapping data: application to edible crabs, Cancer pagurus, on the east coast of England. Fisheries Research 65, 361-378. Bennett DB. 1995. Factors in the life history of the edible crab (Cancer pagurus L.) that influence modelling and management. ICES Marine Science Symposium 199, 89-98. Bennett DB, Brown CG. 1979. The problems of pot immersion time in recording and analysing catch-effort data from a trap fishery. Rapp. P.-v. Reun. Cons. int. Explor. Mer. 175, 186-189. Busby MS, Mier KL, Brodeur RD. 2005. Habitat associations of demersal fishes and crabs in the Pribilof Islands region of the Bering Sea. Fisheries Research 75, 15-28. Byers JA, Anderbrant O, Löqvist J. 1989. Effective attraction radius: a method for comparing species attractants determining densities of flying Insects Journal of Chemical Ecology 15, 749-765. Collins M, Yau C, Guilfoyle F, Bagley P, Everson I, Priede I, Agnew D. 2002. Assessment of stone crab (Lithodidae) density on the South Georgia slope using baited video cameras. ICES Journal Of Marine Science 59, 370-379. Hilborn R, Walters C. 1992. Quantitative Fisheries Assessment: Choice, Dynamics and Uncertainty Chapman and Hall, New York. Himmelman J. 1988. Movement of whelks (Buccinum undatum) towards a baited trap. Marine Biology 97. Hughes D, Atkinson RJA. 1997. A towed video survey of megafaunal bioturbation in the north-eastern Irish Sea. J. Mar. Biol. Ass. UK 77, 635-653. Karlsson K, Christiansen ME. 1996. Occurence and population composition of the edible Crab (Cancer pagurus) on the rocky shores of an islet on the south coast of Norway. Sarsia 81, 307-314. McQuinn I, Gendron L, Himmelman J. 1988. Area of attraction and effective area fished by a whelk (Buccinum undatum) trap under variable conditions. Can. J. Fish. Aquat. Sci. 45. Melville-Smith R. 1986. Red crab (Geryon maritae) density in 1985 by the technique of effective area fished per trap on the northern fishing grounds off southwest Africa. S. Afr. J. Mar. Sci. 4, 257-263. Miller R. 1975. The density of the commercial spider crab, Chionoecetes opilio, and calibration of effective area fished per trap using bottom photography. J. Fish. Res. Board Can. 32, 761-768. Miller RJ. 1989. Catchability of American lobsters (Homarus americanus) and Rock crabs (Cancer irroratus) by traps. Can. J. Fish. Aquat. Sci. 46, 1652-1652.

11 Miller RJ. 1990. Effectiveness of Crab and Lobster traps. Can. J. Fish. Aquat. Sci. 47, 1228- 1251. Miller RJ, Addison JT. 1995. Trapping Interactions of Crabs and American Lobster in Laboratory Tanks. Canadian Journal of Fisheries and Aquatic Sciences 52, 315-324. Morello EB, Froglia C, Atkinson RJA. 2007. Underwater television as a fishery-independent method for stock assessment of Norway lobster (Nephrops norvegicus) in the central Adriatic Sea (Italy). ICES J. Mar. Sci. 64, 1116-1123. Munch-Petersen S, Sparre P, Hoffmann E. 1982. Abundance of the shore crab, Carcinus maenas (L.), estimated from mark-recapture experiments. Dana 2, 97-121. Ricker WE. 1975. Computation and Interpretation of Biological Statistics of Fish Populations. Sainte-Marie B, Hargrave B. 1987. Estimation of scavenger abundance and distance of attraction to bait. Marine Biology 94, 431-443. Shelton JH, Ransom, A. M., and Dunn, A. 2001. Is catch-per-unit-effort proportional to abundance? Can. J. Fish. Aquat. Sci. 58, 1760-1772. Skajaa K, Ferno A, Lokkeborg S, Haugland EK. 1998. Basic movement pattern and chemo- oriented search towards baited pots in Edible crab (Cancer pagurus L.). Hydrobiol. 372, 143-153. Stevens BG. 2003. Timing of aggregation and larval release by Tanner crabs, Chionoecetes bairdi, in relation to tidal current patterns. Fisheries Research 65, 201-216. Tuck ID, Chapman CJ, Atkinson RJA, Bailey N, Smith RSM. 1997. A comparison of methods for stock assessment of the Norway lobster, Nephrops norvegicus, in the Firth of Clyde. Fisheries Research 32, 89-100. Turchin P, Odendaal FJ. 1996. Measuring the effective sampling area of a pheromone trap for monitoring population density of southern pine beetle (Coleoptera: Scolytidae). Environmental Entomology 25, 582-588. Wolff M, Soto M. 1992. Population Dynamics of Cancer polyodon in La Herradura Bay, Northern Chile. Marine Ecology Progress Series 85, 69-81. Östrand F, Anderbrant O. 2003. From where are insects recruited? A new model to interpret catches of attractive traps. Agricultural and Forest Entomology 5, 163-171.

12 V

Stock indicators of the edible crab (Cancer pagurus) in the Kattegat and Skagerrak estimated by length cohort analysis and resampling of growth parameters

1Ungfors, A*. and 2Ulmestrand, M

1Department of Marine Ecology - Tjärnö, University of Gothenburg, 452 96 Strömstad, Sweden +46 526 686 88, [email protected] 2Institute of Marine Research, National Board of Fisheries, 453 21 Lysekil, Sweden

Corresponding author: Anette Ungfors, [email protected], +46 526 686 88

1 1 Abstract

In this study we estimate the von Bertalanffy growth parameter L using length frequency in catches (Power-Wetherall approach) and the K by the use of growth data from a mark- recapture experiment (a forced Gulland-Holt plot, Munro, Fabens, Appledoorn in FISTAT II, and a Ford-Walford plot) for females and males in Skagerrak and Kattegat, respectively. The stock indicators fishing mortality, current stock biomass and abundance are calculated for the female and male stock in Skagerrak and Kattegat by Monte Carlo resampling of growth parameters and weight-at-length and length cohort analysis (LCA) (Matlab 7.5). In addition, the egg production is estimated, based on knowledge of fecundity (resampling procedure within regression distribution), female stock abundance and an estimate of the spawning proportion. The fishing mortality was higher for females than for males, and the fishery in Kattegat exploits larger individuals whereas the fishery in Skagerrak seem to have a wider exploitation pattern. The mean fishing mortality Fall and the Fp is around 0.3 for females and 0.2 for males. Overall, the fishing mortality seems to be low. Based on total commercial and estimated recreational landing of 401 tonnes in Kattegat and Skagerrak, the estimates on the current stock was ranging between 1600-2600 tonnes or 4-8 million of edible crabs, and the egg production was around 5-7x10^11. These ranges of stock indicators consider different values on growth parameters and natural mortality (M). A lower M generated a lower stock abundance and egg production whereas a higher M generated higher stock indicators. Natural mortality had also an impact on the estimated fishing mortality. We discuss the advantages and disadvantages of the used stock assessment approach.

Keywords: von Bertalanffy growth parameters, Monte Carlo resampling, length cohort analysis, fishing mortality, stock biomass, egg production

2 2 Introduction Sustainable resource exploitation needs information indicating the stock´s ability to withstand fishing and natural mortality to grow and recruit fulfillingly in the long term. An important indicator is the fishing mortality coefficient (F), which is an estimate on the proportion of the stock dying due to the fishery. Other indicators are e.g. stock abundance, spawning biomass, juvenile biomass and egg production, which are estimates of stock status or recruitment potential. For these indicators target and limit reference points, are empirically and scientifically established for valuable exploited stocks. To avoid growth overfishing i.e. fishing too small juvenile individuals the fishing mortality FMSY where the yield of the stock is maximised (MSY), is a target to be obtained, or rather a limit not to exceed. Avoidance of recruitment overfishing i.e. fishing to hard on mature individuals who give rise to next generation is harder to avoid as the relationship of the spawning stock and consequential recruitment is complex.

Direct visual observation on abundance in marine habitat is often more effort demanding compared to observations of terrestrial species because of the 3D and low transparency of the oceans. The recent development and availability of new techniques such as echo-sounder, cameras on trawls and remotely operated vehicles (ROV), make visual methods possible below the water surface. However, estimation of the abundance of marine species is often based on calculations (assessment) of the population, restricted to underlying assumptions of recruitment, natural mortality, immigration and emigration. Today there exist several models for crustacean stock assessment all with their pros and cons (Smith&Addison 2003), and the usefulness is dependent on the existing data and the fishing history. A fishing history of a large decrease in abundance are informative for stock assessment, and the quotation of John G. Pope ’the more fish you catch, the better you know how many there were‘ summaries the findings of informative data for abundance and reference points in a recent paper of Magnusson and Hilborn (2007). Contrast in harvest rate seemed to be of secondary importance. Schnute et al. (2007) enlighten the problem with many models and different computer languages resulting in difficulties not only to compare stock status but as it involves a decreased availability to management. General production models (logistic growth of biomass) using time-series of abundance indices of the stock and total effort or total landing, have now evolved into more dynamic age or size-structured models. For example the assessment models of Blue crabs Callinectes sapidus (Kahn&Helser 2005; Miller et al. 2005) use catch-surveys for recruits and adults to add recruitment information and stochastic growth i.e. using probabilities for growth into another length class have also been considered (Siddeek et al. 2004; Bunnell&Miller 2005). In these models it is possible to solve different involved parameters as recruitment, natural, handling and fishing mortality, and risk assessment have been included (Zheng et al. 1995; Punt&Kennedy 1997; Zheng et al. 1997).

Models as delay-difference, depletion and virtual population models are shown to be special cases of a generalized age-structured model (references within Magnusson&Hilborn 2007). Virtual population analysis (VPA) is the procedure for determining the amount of individuals there must have been in the sea to account for the known catch and the natural losses as mortality. Age-based population analysis (APA) (Pope 1972) is an approximation to, and computationally simpler than VPA. The main difference between VPA and age cohort analysis is that the exponential decline in numbers within any age class in VPA, is changed to a step-wise decline in cohort analysis meaning that the catch is caught half-ways through the age interval. Natural losses decline exponentially in VPA and APA. For species with

3 3 difficulties in age determination caused by homogenous climate with no annular striation in otoliths or scales such as in tropic fishes, or by the lack of calcified structures and repeated moults such as in crustaceans, length cohort analysis (LCA) (Jones 1984) have been used (Addison&Bennett 1992; Wolff&Soto 1992; Kirchner 2001; Ulmestrand&Eggert 2001). However, over the last decade aging technique using lipofuscin age-pigment accumulation rate in the brain or eye-stalks has been established. Ageing have been performed for several marine and fresh waters decapods including the edible crab Cancer pagurus (Sheehy&Prior 2005) but also e.g. Callinectes sapidus (Ju et al. 2001), Homarus gammarus (O'Donovan&Tully 1996; Sheehy&Bannister 2002), Homarus americanus (Wahle et al. 1996), Nephrops norvegicus (Tully 1993), Pacifastacus leniusculus (Belchier et al. 1998; Fonseca&Sheehy 2007), Panulirus argus (Maxwell et al. 2007) and Cherax quadricarinatus (Sheehy 1992). Also, aging initiatives using estimations on the inter-moult period by isotopes 228Th/228Ra in the pre-moulted carapace (Latrouite et al. 1991; Verdoit et al. 1999) have been tried.

In this study we assess the edible crab Cancer pagurus stock in Skagerrak and Kattegat with length cohort analysis, using von Bertalanffy growth parameters L and K estimated from length frequency data and mark-recapture experiment. The impact on estimates of i) fishing mortality measured as the average fishing mortality Fall, mean fishing mortality over the inter- quartile F110-160, fishing mortality of the three most exploited cohorts F3max, coefficient of variance, Fp and Fc (fishing mortality standardised for population and catch numbers, respectively see equation 11), ii) current stock biomass and abundances, and iii) the recruitment potential measured as egg production of the spawning stock, are estimated using Monte Carlo resamplings of L using different mean and standard deviation. Resampling is also allowed in the weight-at-carapace width relationship for biomass calculations from stock numbers, and in the fecundity-at-carapace width for egg production calculations. The analyses are performed in Matlab 7.5 (MathWork Inc.). In addition, of the commonly used value of natural mortality of 0.2 the LCA is run for M 0.1 and 0.3. No calculation on long term changes on biomass or yield-per recruit based on simulated effort changes is presented.

In length-cohort analyses the parameters of growth rate is important as von Bertalanffy growth curve (VBGC, relation of size to age) is used for estimation of the time (t) to grow between length cohorts (Jones 1990). The reliability of length cohort analysis is discussed and drawbacks of the model have been stated (Rosenberg&Beddington 1988; Hilborn&Walters 1992; Sheehy&Prior 2005). Efforts on minimizing the model limitations i.e. the discrepancy between size and age have been made by excluding the largest pseudo cohorts with too large variation in size-at-age, and by sensitivity analyses of growth parameters and natural mortality (Jones 1979; Addison&Bennett 1992). Still, LCA is used for relative comparison of yield per effort with different growth parameters (Ulmestrand&Eggert 2001) or used for its simplicity and shortage of alternatives (Wolff&Soto 1992; Kirchner 2001).

4 4 Material and methods Parameter estimation and input data Growth rate is assumed to follow the von Bertalanffy growth curve i.e. a linear decline in growth rate with age, -K(t-t ) Lt= L(1-e 0 ) (equation 1)

where Lt is the length at age t, L the asymptote length where growth rate theoretically is zero and is the mean length an individual would reach if it grew for an infinite number of years, K -1 (yr ) is the Brody growth coefficient, indicating the rate of growth towards asymptote and t0 is the time at zero length.

Pauly (1984) presented a modified formula of Wetherall (1986) method based on Powell (1979) and Beverton and Holt (1956), to estimate L and Z/K from length-converted catch frequency. Wetherall estimated Z in a steady state population with constant exponential mortality from a mean length sample (L) above a selected cut-off point (L´) as Z=K[(L-L)/L- L´)]. For a series of arbitrary cut-off lengths (Li´) above size of full recruitment to the fishery and corresponding mean lengths of all individual above Li, there is a linear relationship shown below according to Pauly (1984),

Li-Li´=+Li (equation 2)

Y-values of the difference between mean length and cut-off point is plotted against cut-off points to judge linear relationship. and is then estimated by linear regression of the selected length class range, and L = -/ and Z/K=(1+)/-. Estimations on L are also performed by the method of Munro (Munro 1982), Faben (Fabens 1965) and Appeldoorn (Appeldoorn 1987) respectively (FISAT II).

For individuals larger than length at onset of sexual maturity von Bertalanffy growth curve assume that the growth rate (dL/dt) declines linearly with length, and Gulland and Holt (1959) showed that K and L can be estimated using the relationship L/t= a + bL (equation 3)

where L=L2-L1, t=t2-t1 and L=L1+(L/2), and K and L is estimated as K=-b and L= - a/b. The estimation of L from the Powell-Wetherall method is used to fix (“force”) the line to the x-axis through the data points of L/t, to be able to calculate the linear regression coefficients and K. The growth data comes from mark-recapture experiments where edible crabs in Skagerrak and Kattegat have been marked with suture tags and Floy (Ungfors et al. 2007) tags allowing for recapture of tagged individual after carapace shedding and growth . Data on moult increment and time between tagging and recapture exists from the 1968-1973 marking period in Skagerrak where in total 3749 edible crabs were tagged and released (moult increment Hallbäck, unpublished). Of these, 1250 individuals (33 %) were recaptured and 126 individuals indicated growth. In order to decrease the risk of over-estimation of growth due to short time since release, only recoveries longer than one year ( 365 days) were considered. Underestimation of growth is considered by not including the recaptured individuals with

5 5 zero growth, and < 5 mm due to measurement errors. Thus, 54 females and 12 males are used in the growth analyses of L/t (nfemales=54, nmales=12). K are also estimated by the iterative Munro (Munro 1982), Fabens (Fabens 1965) and Appledoorn (Appeldoorn 1987) method in

FISAT II, and by the Ford-Walford plot where L is set to 210, 200 and 190 mm and the sex- specific average of L/t is used to calculate K (Jones 1984).

The parameters a and b in equation W=aCWb, where W=weight (g) and CW=carapace width (mm) were solved by linear regression of log transformed weight and carapace data. Weight- at-carapace width is used in the calculation of biomass from number of individuals. Weight data are restricted to include only landed crabs of good meat yield.

Estimations on natural mortality rate (M) are performed by the aid of two general life-history 0.72 formulas: 1) Rikhter&Effanov formula where M=(1.52/tmass) -0.16, where tmass is the age (year) at which 50% of the stock reaches the age of “massive spawning”. M is estimated for massive maturation age between 4 and 8 years. 2) Pauly (1980) ln(M)= -0.0152-0.279 log(L) + 0.6543 log(K) + 0.4634ln(T) and -0.4852-0.0824ln(W) + 0.6757 ln(K) + 0.4627ln(T) where W is the weight (g) at L and T is the mean annual habitat temperature. Temperature data from monthly samplings at 30 m depth from 15 locations along the Skagerrak coast (www.bvvf.se), annual average 9.2 °C for 2007.

A discrete growth curve based on measurement on moult increment (MI) per pre-moult CW (tagging experiment, laboratory moultings and creel captures of moulted individuals within creels) and moult frequency based on literature on C.pagurus (Edwards 1979) and C. magister (Wainwright&Armstrong 1993) are given to show carapace width with age. 25 to 10 % of MI per premoult carapace width is used (25% < 130 mm, 20% 130-150 mm, 15 % 150- 170 and 10 % > 170 mm). The combination of growth parameter, which makes the continuous Bertalanffy growth curve performance similar to this guess of discrete growth, is given.

Length frequency data Length frequency is sampled from commercial landing and discards in Kattegat and Skagerrak (figure 1). Samplings have covered the fishery distribution at coastal and more offshore ground in Kattegat and at coastal locations in Skagerrak. During the years 1999 to 2004 some locations have been resampled up to five times and other have been visited only occasionally. In addition to the capture data sampled by an observer on selected trips a few fishermen have been filled out capture log books for three pots on a regular basis during 2002-2004. The sampling months are from May to December. In total, 19322 edible crabs have been measured in samplings considering both landing and discard frequency for females and males, respectively (table 1).

The total landing of edible crab in Kattegatt and Skagerrak (table 1) is used to raise the sampled length frequency of landings and discards (figure 2). A mortality of 1 % of the discards was used to calculate removal frequency from raised landings and discards (table 2). The total commercial landing in 2006 was 134 tonnes (log book data, National Board of Fisheries) and the recreational fishery in 2006 was estimated to 269 tonnes (Anon 2007).

6 6 Commercial landing was similar for the Kattegat and the Skagerrak but recreational landings were 53 and 216 tonnes, respectively (Anon 2007). In addition to fishing area, the landings were divided into a female and male part: 1:1 of females to males are assumed in Skagerrak and 2:1 in Kattegat, which is based on sex ratio in the samplings. The fishery in Skagerrak is coastal but in Kattegat it occurs also further offshore with a different capture composition (larger individuals) why half of the commercial landing are assumed to be of inshore length frequency and half of offshore (sex-specific). All recreational fishery in Kattegat was assumed to be coastal (table 1).

Length cohort analysis (LCA) The calculation steps of LCA are describe in Jones (1984) and a recent user-friendly description of length cohort analyses is presented by Jennings et al (2001, p. 143-144). Length cohort population analysis is based on the formulas of age cohort population analyses (Pope 1972) but instead of using the frequency of different age cohorts (often 1 year in between) of catch or landings and discards, the frequency of length groups with constant class interval are sampled. The underlying assumptions are that the majority of the decline in the length class is due to the catch (fishing mortality), and that the length composition of the catch is in a steady- state condition caused by constant (i.e. no time trends in) recruitment and mortality.

The age (t) of the length groups are then calculated with aid of growth parameters L and K, and von Bertalanffy growth equation (von Bertalanffy 1938; Beverton&Holt 1957) solved for t, t1= -(1/K)*ln(1-(L1/L)) (equation 4)

where t1 is the age of the smallest cohort, t2 the age of next cohort etc. The time for growth to next cohort, t, is calculated as the difference in ages or as

t=(1/K) ln((L-L1)/( L-L2)) (equation 5)

where L1 is shortest width of cohort 1 and L2 shortest width at cohort 2. Age cohort and length cohort analyses use Pope´s approximation (Pope 1972) of the catch equation of virtual population analyses (VPA), assuming that the catch is taken halfway through the age of the cohort instead of continuously. Jones (1984) modified Pope formulas for LPA, and both formulas are given below. The number of individuals per cohort is calculated by Mt/2 Mt/2 Nt= (Nt+te + Ct) e (Pope, equation 6)

Mt/2 or as Jones (1984) noted that Mt/2= (M/2K)*ln((L-L1)/( L-L2)) and e = (L-L1)/( L- M/2K L2) = XL2L1, then a simpler numerical formula for the step-wise backward calculation of number attaining each size class, if considering catch and natural mortality, is

NL1=(NL2XL2L1+C1,2)XL2L1 (Jones, equation 7)

However, first is the number attaining the largest cohort calculated by the use of an initial guess of the terminal F/Z in the catch equation, and solving for NL -Zt CL = F/Z *NL(1-e ) (equation 8)

7 7 keeping e-Zt =0 as the age of the largest size class after the t is infinite. After being able to calculate the stock size attaining each length class, the fishing mortality rates for each cohort can be calculated by F=M*((F/Z)/(1-F/Z)) (equation 9) where F/Z per cohort is calculated as the quota from catches and the total decrease in stock numbers

F/Z = C1,2/(NL1-NL2) (equation 10)

The fishing mortality is also presented as the weighted for population (Fp) and catch weight (Fc) as suggested by Bannister and Addison (1984),

Fp=(Pi Fi ti)/( Pi ti) and Fc=(Ci Fi ti)/( Ci ti) (equation 11)

To calculate the actual numbers in the stock at Sea from the numbers of individuals that attain each cohort, the average number per length class and year is calculated as

NL1L2 = (NL1-NL2)/Z (equation 12) where Z is calculated as Z=M/(1-F/Z) (equation 13)

Monte Carlo simulations of LCA

The LCA is accomplished in MAT LAB computer programme. Indata for L is drawn randomly with replacement by Monte Carlo simulation from a normal distribution with a defined mean and standard deviation. The mean and standard deviation, 202.2 ±12.2 females and 197.4±8.6 males, is estimated from the calculated values of L but other means and standard deviations are controlled for. A minimum L was set to 191 mm to allow LCA calculations with the plus group of 190 mm. As the L and K are linked (covariates) the K is drawn from the linear relationship, based on the simulated L and the slope (-0.006349), standard deviation (0.0004) of the slope and intercept (1.589) (figure 4). A minimum of K was set to 0.150. 1000 runs of the LCA with different values within the L distribution and dependent K combinations are performed to estimate fishing mortality with uncertainty (SD or 95% confidence interval) for females and males in Skagerrak and Kattegat respectively. The same L and K is used for all eleven cohorts (plus group excluded) in a run.

The biomass of the stock is calculated by using the linear log-log relationship between crab weight (g) and carapace width (mm) log(W)=log(a) +log(CW)*b to estimate weight at mid cohort length, and multiplication by the cohort-specific average number of edible crab. The parameter value log(a) and b is estimated in each LCA run (1000) by Monte Carlo simulation using the distribution of mean and standard deviation given in table 3 (specific parameter values for females and males in Kattegat and Skagerrak, respectively). The stock biomass

8 8 (tonnes) is given per cohort class or as a mean, with standard deviation or 95% confidence interval calculated from the 1000 runs.

Estimation of egg production of the spawning stock biomass build on: 1) data of the egg production (fecundity) for female edible crab in Skagerrak and Kattegat, fecundity (no.)=24180*CW-2229266 (standard deviation slope 2739; standard deviation intercept 417142) (Ungfors 2007). The mid carapace width per cohort is used to draw a value of fecundity given the regression characters above; 2) on the assumption of a knife-edged start of spawning at the 110 mm CW cohort (113 mm CW smallest ovigerous female) (Ungfors 2007), and 3) estimations of the annual proportion of spawning females of the female population. Observations of the ovigerous proportion (Hallbäck, H unpublished) show that at most females are egg-bearing every second year as the proportion mature based on this character reach 50%: P115=0.01, P125=0.05, P135=0.15, P145=32, P155=44, P165=0.48, P175=0.50, P185=0.50. The total egg production is estimated through the product of the number of females per cohort (estimated in the LCA runs), and the cohort-specific fecundity randomly simulated from the regression times the proportion ovigerous females.

Standard deviation or 95 % confidence interval is presented for the different averaged and standardised F, stock estimates and egg production. The coefficient of variation (CV), which is the standard deviation divided with its mean, is also used in presentations of fishing mortality.

Results Growth parameters

The estimations of L and K from different approaches are given in table 3. A mean and standard deviation of L is estimated from these values of L; for females 202.2± 12.2, and for males 197.4±8.6. For graphical presentation on the length at age for the different growth parameters a selection of the estimated combinations of growth parameters (7 of 11 combinations for females and 7 of 9 combinations for males) from table 3 are inserted in Bertalanffy growth curve (VBGC) (figure 3a and b respectively). In figure 3c) is a guessimate for the discrete growth curve based on measurements on Swedish edible crab moult increments per pre-moult CW, and from moult frequency based on literature on C.pagurus (Edwards 1979) and C. magister (Wainwright&Armstrong 1993). A continuous VBGC with L of 217 and K of 0.160 fit relatively well to this discrete growth curve. The growth parameters are not independent but co-vary in such that a higher L generates a lower K for the used approaches. The linear regression between K as a dependent variable and L as the 2 independent (figure 4, K= L*-0.0063+1.5895 with SD ±0.0004 of the slope, R =0.37) was used to calculate K from L in further simulations on LCA in MATLAB.

Fishing mortality (F)

The overall fishing mortality, the average for the three most exploited cohorts F3max, F110-160, and F weighted to population (Fp) and to catch (Fc) is given in table 4. Females are more exploited than males, which is a consistent pattern for Kattegat and Skagerrak (table 4, and figures 5 and 6).

9 9 The cohort-specific fishing mortality has a different pattern in Kattegat in comparison with Skagerrak. In Kattegat F is relatively low for the cohorts up to 140 mm CW and rise sharply for cohorts 160-170 mm CW (figure 5). In Skagerrak the increase in F with size is smoother including a wider range of cohorts i.e. 140-170 mm CW being most exploited (figure 6).

Changes in input mean and standard deviation of L impacts the coefficient of variance (CV) of fishing mortality more than it impacts actual changes in fishing mortality (figure 7). A low mean (202 mm CW) results in a relative high CV of the larger cohorts (approx. 60%) and lesser CV in the smaller cohorts. A high mean of 217 mm CW increase the CV on the smaller cohorts (50 % CV of the smaller and 40% CV of the larger cohorts) (figure 7a and b). Ten times lower standard deviation of the low input L decrease the CV for the large cohorts (figure 7a and c). Narrowing the distribution around the large mean of 217 mm CW does not impact the relative standard deviation much in comparison with a wider distribution (figure 7b and d) except for a small increase in the smaller cohorts.

Values of natural mortality within 0.1-0.3 have no dramatic effect on mean fishing mortality (M0.1 0.32±0.14, M0.2 0.30±0.11 and M0.3 0.28±0.12) but an overall increase in CV is noted with higher M especially for the smaller cohorts (figure 8, Kattegat females as an example). The three most exploited cohorts i.e. 150-170 mm CW has mean F3max of 0.78±0.25, 0.71±0.26 and 0.65±28 with increasing M.

Stock abundance and egg production The total stock biomass in Kattegat and Skagerrak estimated with LCA is 2495±613 tonnes and a stock abundance 6.03±1.1 million of edible crabs (table 5a). Using higher mean L in the resampling procedure resulted in 20 % lower biomass and 4 % lower abundance (table 5b). The egg production is five magnitudes higher than the stock abundance. The total egg production of the spawning stock is 6.79±2.38 x10^11 but 14 % lower if using a higher value on L (table 5). An example (Females Skagerrak) of the cohort specific outcome of stock and egg estimates for the 1000 runs are shown in figure 9, and averaged in table 6.

Assuming a natural mortality of 0.1 results in lower estimates of stock size and egg production and using a higher (0.3) result in higher estimates (table 6), compared to the general used M of 0.2 (table 5). The stock is 1599±221 tonnes or 4.32±0.38 x10^6 crabs, and the estimated egg production is 5.04±1.33 x10^11 when M=0.1, and 2619±467 tonnes or 8.29±1.25 x10^6 crabs and 6.90±2.63 x10^11 eggs when M=0.3 (compare with table 5b for M=0.2).

10 10 Discussion

We have estimated von Bertalanffy growth parameter L and K for the edible crab in Kattegat and Skagerrak. These parameters were used in LCA for the estimation of stock indicators fishing mortality, stock biomass and abundance and egg production of spawning stock. Below we compared our result with findings in crustacean literature. In addition we discuss the importance of natural mortality and strategies for length frequency sampling. The context of the discussion considers the advantages and disadvantages of using LCA. The advantages are that the model use length frequency data available for crustaceans for which aging methods are in its infancy. Species for which aging is a problem this model still is an assessment option for rough estimates of e.g. stock abundance. Also the model can be compiled in common and user friendly programmes as Excel. However, we performed the LCA in MATLAB as we included uncertainty of growth parameters, weight-at-length and fecundity by Monte Carlo resampling. The drawback of the model is that length is used as an indicator of age, but that the individual growth has been shown to be variable. Furthermore, the parameter natural mortality has a large impact in the model.

Growth parameters and LCA

Our analyses of length frequencies pointed at L of 179-212 mm but as the maximum observed edible crab in Swedish waters is 207 mm CW, the lower estimated L might be biased by few captures of large individuals. Our estimate of L 217 mm, 5 % over maximum carapace width, is considerably lower than the chosen L of 240 mm at the east coast of England (Addison&Bennett 1992). However, Addison and Bennett (1992) considered values of 220 and as low as 180 mm for the UK stock assessment. The Addison and Bennett (1992) best estimate of the growth parameter K is 0.191 and 0.196 for females and males respectively. These estimates originating from tagging data and using Jones modification of a Ford-Walford plot, is close to our estimate of K for the same approach, especially for females. However, our estimations of growth parameters by Ford-Walford gave lower value for K in comparison with approaches in FISAT II (forced Gulland-Holt plot, Munro, Fabens, Appledoorn). Haddon (2001, p. 212) point at discrepancies of growth parameter from different approaches: L from tagging data e.g. Fabens method are shown to be biased high, but low for the K parameter in comparison with fitting VBGC by length at age data where both parameter were slightly lower than the overall averages. Sheehy and Prior (2005) estimated growth parameters with fitting Bertalanffy growth curve to weight at age data for edible crab, and the parameters were within the range of most previously stock assessment options: L 176-245 and K 0.41-0.66. The K parameters from that study are at the higher end of the interval we found, 0.193-0.586. A continuous Bertalanffy growth curve with L of 217 and a K of 0.160 graphically seem to fit relatively well with a empirical discrete growth curve based on estimates on the proportional MI (Swedish data; Hallbäck, unpublished) and moult frequency (Edwards 1979; Wainwright&Armstrong 1993). By lipofuscin aging technique Sheehy and Prior (2005) estimated the average maximum edible crab life-span to around 10 years around UK and oldest crabs were around 14.6 (95 % CI 11.5-19.1). Interestingly, a 207 mm CW crab have an estimated age of 19.2 years based on the length-based VBGF as in LCA, using L 217 and K 0.160. Sheehy and Prior (2005) showed that the longevity varied inversely with sea temperature i.e. a longer life at the cooler E. coast than in the warmer Channel. We can only speculate on longer longevity further north such as in in Kattegat and Skagerrak.

11 11 The fishing mortality in Kattegat and Skagerrak is higher for females (average F110-160=0.33, Fp=0.26 and Fc=0.53) than for males (average F110-160=0.22, Fp=0.21 and Fc=0.35). From these values of F the annual fishing mortality rate i.e. proportion of the stock dying from fishing, is estimated to 23-41 % (F 0.26-0.53) of females and 19-30% (F 0.21-035) for males. In general, are females the preferred target for Swedish fishermen as the price for females is higher than for males, which may explain this exploitation pattern. Possible, catchability is higher for females e.g. as females are highly attracted to baited pots after winter diet and hatching period (Brown&Bennett 1980). In contrary, fishing mortality on the UK East coast, from LCA, has been found to be lower for females (average Fp and Fc=1.30) than for males (average Fp and Fc=1.62) (Addison&Bennett 1992). If excluding the Norfolk data (one of three analysed regions) these estimates are 0.83 and 0.50 respectively. The Fp value for Kattegat and Skagerrak ranged between 0.17-0.27 and the Fc between 0.22-0.61 whereas similar estimates for the East coast of England is 0.34-3.02 and 0.66-3.36, respectively. Recent findings on the UK East Coast, using age-length key, linearized catch curves (Z) and estimations on natural mortality (M), show that fishing mortality (F=Z-M) on female were higher than that for males (Sheehy&Prior 2005). For the Western English Channel, Sheehy and Prior (2005) found that mortality induced by the fishery is higher (1.02) for males than for females (0.21), whereas Bennett (1979) found more consistency in fishing mortality between sexes (0.44-0.46) using length frequency data converted to age data and exploitation estimates from tagging. An impact of the growth parameters on the coefficient of variance of fishing mortality is observed e.g. a low L in combination with a relative wide SD generates higher CV for the larger cohorts. However, the fishing mortality in Kattegat and Skagerrak is low despite consideration (resampling) of different potential parameter values. Addison and Bennett (1992) found that the fishing mortality Fc varied between 0.57-0.78 for females and 0.83-1.54 for males, for six different growth parameter combinations. The fishery mortality in Kattegat and Skagerrak seem to be in the lower range of estimates from other areas.

Uncertainty in growth parameters K and L is judged to be the major cause of poor length based assessment for Nephrop norvegicus Skagerrak-Kattegat stock (ICES 1999). Sensitivity analyses for different combinations of growth parameters were performed in Addison and Bennett (1992) LCA for yield and biomass per recruit, respectively. In our estimation of stock biomass and abundance a wide range of growth parameters were considered using Monte Carlo resampling of L around a mean with a given standard deviation. In addition the K was resampled from the regression of K and L with uncertainty in the slope. Given the total commercial and recreational landing of 401 tonnes, the stock biomass is 1600-2600 tonnes in Kattegat and Skagerrak, and the abundance about 4-8 million crabs. This stock estimation must be considered minimum as the actual commercial landing is probably higher than reported. Critizism on using size bins as pseudo age cohorts in LCA base its arguments on that the majority of size variation is not explained by age and that the descending slope of the CW-frequency distribution used in LCA is primarily a reflection of individual growth variation rather than age (Sheehy&Prior 2005). The individual variation of growth is large but we believe that the right-hand slope indicate a decreasing abundance of older individuals. A high variation in individual growth is to some extent regarded for in the average results, by repeating the LCA several times (1000) using different growth combinations per repeat. The precision of age estimates of 1, 7 and 15 years old edible crabs, using 95% confidence interval, is 0.6-2, 5.2-9.7 and 11.8-19.7 (Sheehy&Prior 2005). So, using lipofuscin aging in stock assessment still incorporates bias, similar to the drawback of using length frequency as estimates of age bins.

12 12 The approaches of the age determination of crustaceans are still expensive and time- consuming but age-length keys have recently been used in parameter estimation and stock assessment (Ju et al. 2003; Sheehy&Prior 2005; Fonseca&Sheehy 2007). Crustacean assessment based on both age and length-cohort approaches for the same regional area have been used to evaluate the traditional length-cohort method (Sheehy&Prior 2005; Fonseca&Sheehy 2007). The ability to use lipofuscin frequency distribution more accurately estimates (lower prediction errors, higher regression r2) the age distribution in the population in comparison with the size distribution, which generally is considered a poor proxy for age because of individual variations in growth due to numerous environmental, density- dependent, and fishery-related factors. However, for some environment, size can be a predictor of age (Uglem et al. 2005) and even for a long-lived species as the freshwater signal crayfish Pacifastacus leniusculus with longevity of 12-16 years the r2 of size and age is 84.1 % (Belchier et al. 1998). Lipofuscin aging technique has shown that there is large individual variation in size-at-age but importantly the mean age is increasing with larger sizes.

Recommendations to define the plus group to less than 70 % of L (Addison&Bennett 1992) were not considered. We suspect that exclusion of larger individuals negatively bias the stock estimation as including does.

A larger total egg production was seen with a smaller L (mean 202). A smaller mean L generates larger K parameter values i.e. individuals grow faster, mature earlier and therefore produce more eggs during their life-time.

Natural mortality The importance of an accurate estimate of natural mortality is well-known in fisheries assessment, and as well is the difficulty estimating it. Our assessment is no exception, the natural mortality impacted the stock estimates and the average fishing mortality i.e. the stock abundance and egg production increased with higher value on M but the fishery mortality decreased. Evaluation of long-term harvest strategy for red king crab Paralithodes camtschaticus using length-structured model found that the result was highly sensitive to changes in M of 0.2-0.3 (Zheng et al. 2003). The fishing mortality is estimated for the blue crab in Cheasapeak Bay given presumed levels of M (Miller et al. 2005). The levels of M produced varying estimates of F with the lowest values being associated with an M of 0.375 and the highest F with an M of 1.2. Natural mortality can usually be estimated by relative abundance of different ages (or size, if aging difficulties) on an unfished virgin population before fishing is impacting age or size structure and where total mortality Z is allocated to M. A review of six common methods for the estimating of natural mortality is given in Quinn and Deriso (1999): 1) catch curve analyses, 2) length-frequency analysis, 3) mark-recapture experiments (Siddeek et al. 2002; Frusher&Hoenig 2003), 4) collection of dead organisms, 5) fitting population models (Zheng et al. 1997) and 6) meta analysis of life history. An alternative to the complex estimations for finding M especially of data poor populations is to use estimations for same species but in other regions, or from other species with similar life- history (alternative 6 above). This value is of course dependent of the accuracy of that estimation and how similar the taxa life-history. General indirect methods, relying on parameters such as age at maturity, longevity, body size, L and K often measured in biological studies, have been established (Hewitt et al. 2007). We estimated M by Pauly (1980) formula using L, K and mean habitat temperature to 0.26, and by Rikther&Efanov

13 13 formula (1976) using age at massive maturation to 0.18-0.34. Based on Hoenig (1983) general formula ln(M)=1.44-0.982Ln (Amax) and using the oldest 5% for the average longevity, Sheehy and Prior (2005) estimated natural mortality to 0.45 for males and 0.39 for females in region E. coast.

Previous edible crab assessment values of M have been in the range 0.1-0.69 (Hancock 1975; Bennett 1979; Addison&Bennett 1992; Sheehy&Prior 2005) but 0.2 are often regarded as a good estimate. Our indirect life-history estimates of M point at M in the mid of this range, or just above the holy 0.2 value. Natural mortality can formerly have been underestimated because of a belief on low predation in the armoured species and a belief in relatively low mortality during moulting. On the other hand, by the use of the general formulas empirically based on several species the edible crab must be considered a rigid species. Not only because of an armoured shelter from predation but from less-active winter (both sexes) and spawned (females) behaviour. Overestimation of M in rigid species by these general life-history formulas might therefore occur.

Sampling strategy of length frequency Internal cycles as moulting and spawning impact the catchability of edible crabs in the fishery why the length frequency during the year may change at a fishing location (Brown&Bennett 1980). Immigration into and emigration out from a location of adult individuals, especially females, may also impact size frequency (and age frequency). Juveniles and pre-recruits may also change habitat during growth. To get a rigid estimation on length frequency in landings it is more efficient to sample one or few pot from all trips from several fishermen instead of several pots from a few trips (McGarvey&Pennington 2001; Woll et al. 2006). The least efficient sampling strategy was by research sampling measuring all pots on selected trips (McGarvey&Pennington 2001). The length frequencies in our study come from a mixture of selected trips with onboard observer measuring whole catch, and from a few fishermen using standardised and/or selected pots for regular measurements. For collection of reliable capture and length data, a sampling strategy must be emphasized from the Swedish National Board of Fisheries allowing observers for edible crab. Or alternatively, fishermen within the pilot projects for local co-operative management of fisheries (Anon 2008) can, if the co-operative initiative become permanent, be encouraged to sample detailed data of one to three pots per fishing trip. Future assessment To use an alternative modelling strategy such as dynamic length-structured method (Punt&Kennedy 1997), we need to evaluate the available data. Biomass surplus modelling (Hilborn 2001) using LPUE data and landings from log-books can be worthwhile testing with data from 1995-2007. The LPUE in the logbooks can be improved by detailed review of the effort reporting by e.g. interviews with skippers to get information on amount of used gears over the years, and possible to get private landing records. Generalized linear models can be used to quantify the variation in LPUE by e.g. year, month, area or vessel/vessel type. Variation in LPUE in the log book due to differences in substrate or depth, can be elucidated by available position of fisheries and GIS information (BALANCE 2007).

Establishing age-length keys for the Swedish edible crab are tempting. The calibration to chronological age and the thermal correction of age estimates for edible crab were made on

14 14 the basis of cohorts modes of neurolipofuscin concentration frequency distributions (NCFD) for different areas with different mean temperatures (Sheehy&Prior 2005), and not by use of individuals of known age reared in laboratory (Belchier et al. 1998). If pronounced temperature differences between Kattegat and Skagerrak fishery locations, keys need to be established for both areas as Sheehy and Prior (2005) found a strong relationship (r2=0.78, p<0.001) between sea temperature and neurolipofuscin accumulation rate.

Acknowledgement We are grateful to Per Jonsson and Mats Lindegarth for invaluable guidance in MATLAB scipt writing and programme instructions. Thanks also to all involved fishermen firstly allowing a female marine biologist onboard and secondly for the measurement support despite delaying working tempo. Hans Hallbäck for scuba diving sampling of ovigerous females used to estimate spawning population proportion.

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20 20 TABLES

Table 1. Length frequencies of edible crab originate from sampling aboard commercial fishing vessels in 1999 to 2004 where both the landed (L) and the discarded (D) individuals were measured. Total landing=commercial landing from logbooks and estimated recreational landing. Stock No. of sampled Total Landings individuals in (tonnes) landing; discard Kattegat F Linsh 1164, Loff 1908; Inshore 57.96; Dinsh 717, Doff 1299 Offshore 22.45=80.41

Kattegat M Linsh 404, Loff 698; Inshore 28.54; Dinsh 282, Doff 565 Offshore 11.055=39.60 Skagerrak F n= 5270; 1874 140.5 Skagerrak M n=4353; 788 140.5 Sum 19322 401

Table 2. Raised removals (no) .per length frequency based on total landing of commercial and recreational per sex and per area, and sampled landing and discard length frequencies. 1 % mortality of the discards was assumed. Total landing Female Male frequency (no.) Kattegat Skagerrak Kattegat Skagerrak 80 1 267 2 361 942 2 977 90 425 510 353 507 100 6 592 3 572 990 5 773 110 4 165 9 837 2 257 13 184 120 8 121 26 174 3 692 25 147 130 18 177 53 009 6 752 44 807 140 28 808 76 374 10 191 45 541 150 40 797 76 121 11 660 46 674 160 35 552 49 783 11 640 37 374 170 16 087 27 403 9 901 29 847 180 3 984 8 289 3 604 15 236 190 1 015 2 608 724 8 346 Sum 164 990 336 041 62 706 275 413 *The sampled length frequencies are scaled to reach the total landings (tonnes) by a multiplying factor using weight-at-carapace width parameters.

21 Table 3. The estimated growth parameters L and K by different approaches, natural mortality M by empirically developed formulas, and weight-at-carapace width. MR=Mark-recapture. Sex Female Male Location Kattegat Skagerrak Kattegat Skagerrak L Capture data 179; 195 193; 212 182; 197, 193; 202 Power-Wetherall (n>140=4308) (n>140=3713) (n>140=1574) (n>140=2649) Z/K 0.92; 2.00 3.28; 5.30 0.82; 1.63 2.12; 2.77 Empirical L 217 (5% over max 207 mm CW) K MR data Forced Gulland- 0.586 (179); 0.403 (193); 0.391 (182); 0.310 (193); Holt 0.386 (195); 0.283 (212) 0.289 (197); 0.266 (202) 0.263 (217) 0.263 (217) 0.214 (217) 0.214 (217) L; K MR data n=54 n=12 Munro`s 201; 0.450 190; 0.603 Fabens 212; 0.253 Appeldoorn`s 210 ± se 16.7; K 0.260±se 0.08) K MR data 0.193 (L 210) 0.241 (L 210) Ford-Walford 0.214 (L 200) 0.269 (L 200) 0.241 (L 190) 0.304 (L 190) M Pauly (1980) 0.21-0.25 (9.2°C) (W-L) 0.21-0.25 (9.2°C) (W-L) Rikther/Effanov 0.34-0.32-0.26- 0.21- 0.18 (age 0.34-0.32 (1976) of 4-8 years at maturation, (age of 4-5 years at maturation, resp.) resp.) Weight –width* n=656 n=716 n=139 n=348 a 0.000194 0.000284 0.00004133 0.00004890 b 2.9297±0.038 2.8620± 0.052 3.2758±0.088 3.2419±0.061 log a -3.71±0.084 -3.55±0.112 -4.38±0.190 -4.31±0.130

*Landings, intact individuals.

22 Table 4. Mean and standard deviation of fishery mortality measured for all edible crab cohorts (Fall), for the inter-quartile 110-160 mm CW (F110-160), for the three most exploited cohorts (F3max) (females and male Skg 150-170 mm cohorts, male Kgt 160- 180 mm cohorts) and the fishery mortality weighted for population, Fp, or catch, Fc, for females and males in Kattegat and Skagerrak. The values of L are simulated by Monte Carlo resampling and the incident value of K is drawn from the regression of K and L (n= 1000 per cohort). Table a) and in b) differ in mean ± SD of the growth parameter L. a) L 202.2±12.2 for females and 197.4±8.6 for males Area Fall F110-160 F3max Fp Fc FEMALE Kattegat 0.26±0.11 0.31±0.12 0.62±0.26 0.26±0.11 0.52±0.23 Skagerrak 0.27±0.12 0.35±0.13 0.57±0.25 0.26±0.12 0.47±0.21 MALE Kattegat 0.19±0.09 0.22±0.09 0.40±0.16 0.22±0.10 0.35±0.18 Skagerrak 0.15±0.07 0.21±0.09 0.27±0.12 0.17±0.09 0.22±0.12 b) L 217±12.2 for females and 217±8.6

Area Fall F110-160 F3max Fp Fc FEMALE Kattegat 0.30±0.11 0.33±0.13 0.71±0.26 0.26±0.11 0.61±0.22 Skagerrak 0.30±0.12 0.35±0.14 0.64±0.25 0.27±0.12 0.54±0.21 MALE Kattegat 0.25±0.10 0.23±0.10 0.58±0.22 0.24±0.11 0.50±0.19 Skagerrak 0.19±0.08 0.24±0.10 0.36±0.15 0.20±0.09 0.32±0.13

23 Table 5. Stock abundance, biomass and egg production of edible crab based on Length cohort analyses. Mean and standard deviation are given (n=1000). Table a) and in b) differ in mean ± SD of the growth parameter L. a) Mean L 202.2 ±12.2 for females and 197.4±8.6 for males.

Stock abundance Stock biomass Current Egg (no.) 10^6 mean (tonnes) production (10^11) KATTEGAT Females 1.05±0.55 329±192 2.44±1.78 Males 0.49±0.38 258±303 SKAGERRAK Females 2.00±1.05 670±419 4.35 ±2.97 Males 2.49±2.44 1238±1538 Sum of means 6.03±1.1 2495±613 6.79±2.38 b) L 217±12.2 for females and 217±8.6 for males. Stock abundance Stock biomass Current Egg (no.) 10^6 mean (tonnes) production (10^11) KATTEGAT Females 1.08±0.64 317±205 2.05±1.57 Males 0.47±0.22 209±175 SKAGERRAK Females 2.07±0.91 617±344 3.82 ±2.22 Males 2.15±1.0 840±522 Sum of means 5.77±0.69 1983±311 5.87±1.89

Table 6. Stock abundance, biomass and egg production of edible crab based on Length cohort analysis. Mean and standard deviation are given (n=1000). L 217±12.2 for females and 217±8.6 for males (as in table 5b). Table a) and in b) differ in used value of natural mortality M. a) M=0.1 Area Sex Stock abundance Stock biomass Current Egg (no.) 10^6 mean (tonnes) production (10^11) KATTEGAT Females 0.82±0.29 254±112 1.82±0.98 Males 0.34±0.12 151±112 SKAGERRAK Females 1.60±0.55 517±269 3.22±1.68 Males 1.56±0.57 677±390 Sum of means 4.32±0.38 1599±221 5.04±1.33 b) M=0.3 Area Sex Stock Stock biomass Current Egg abundance mean (tonnes) production (no.) 10^6 (10^11) Kattegat Females 1.48±0.84 408±245 2.40±1.54 Males 0.70±0.40 279±250 Skagerrak Females 2.95±1.91 845±626 4.50±3.72 Males 3.16±1.84 1087±746 Sum of means 8.29±1.25 2619±467 6.90±2.63

24 FIGURES

Figure 1. Map over sampling locations for length frequency of landings and discards (n=sampled individuals) in commercial edible crab captures.

Figure 2. Raised landing (left) and raised discard (right) size frequency for females and males in Kattegat and Skagerrak.

a) b)

Figure 3. Carapace width-at-age based on a selection of our estimated growth parameters (L and K) for a) females and b) males (see table 3). In c) is shown a simulated discrete growth rate based on moult increment (MI) of 25-10 % (decreasing with size) of pre-moult CW and moult frequency. MI is based on observations on moult of Swedish crabs (tagging experiment and individuals moulted in creels), and estimation of frequency is based on literature of C. pagurus (Edwards 1979) and C. magister (Wainwright and Armstrong 1993) (basically decreasing with size). The dotted line in c) is the von Bertalanffy growth curve with L 217 and K 0.160.

Figure 4. Linear regression of K and L. The standard deviation of the slope is 0.0004. This relationship with including slope uncertainty is used to repeatedly sample K, after that the resampled L is given.

Figure 5. Kattegat. Fishing mortality of a) females using L 217±12.2, and of b) males using L 217±8.6. Cohort 1=80 mm CW and cohort 11=180 mm; 10 mm cohorts. Runs=1000.

Figure 6. Skagerrak. Fishing mortality of a) females using L 217±12.2 and of b) males using L 217±8.6. Cohort 1=80 mm CW and cohort 11=180 mm; 10 mm cohorts. Runs=1000.

a) 202±12.2 b) 217±12.2

c) 202±1.2 d) 217±1.2

Figure 7. Skagerrak females. Fishing mortality and 95 % confidence interval error bars (above), and coefficient of variation (below) for different input mean and standard deviation values of L. In a) L 202 ±12.2, b) L 217±12.2, c) L 202 ±1.2 and d) L 217±1.2. (M=0.2, n=1000).

28 a) b) c)

Figure 8. Kattegat females. Fishing mortality and 95 % confidence interval error bars (above), and coefficient of variation (below) for different parameter value of natural mortality: a) M=0.1, b) M=0.2 and c) M=0.3. The mean±SD of Fall is 0.32±0.14, 0.30±0.11 and 0.28±0.12 for increasing M. L 217±12.2.

Figure 9. Skagerrak females. Mean and 95% confidence interval of stock biomass and abundance, and egg production using L 217±12.2. n=1000.