Reiss Et Al. 2009. Genetic Population Structure Mismatch

F I S H and F I S H E R I E S , 2009, 10, 361–395
Genetic population structure of marine fish: mismatch

between biological and fisheries management units
Henning Reiss1, Galice Hoarau1, Mark Dickey-Collas2 & Wim J. Wolff1
1
Department of Marine Benthic Ecology and Evolution, University of Groningen, Haren, The Netherlands; 2Wageningen
IMARES, IJmuiden, The Netherlands
Abstract Correspondence:
An essential prerequisite of a sustainable fisheries management is the matching of Henning Reiss,
Department of Marine
biologically relevant processes and management action. In fisheries management and
Benthic Ecology and
assessment, fish stocks are the fundamental biological unit, but the reasoning for the Evolution, University
operational management unit is often indistinct and mismatches between the biology of Groningen, Postbus
and the management action frequently occur. Despite the plethora of population 14, 9750 AA Haren,
genetic data on marine fishes, to date little or no use is made of the information, The Netherlands
despite the fact that the detection of genetic differentiation may indicate reproduc-
*The present address
tively distinct populations. Here, we discuss key aspects of genetic population of Henning Reiss is
differentiation in the context of their importance for fisheries management. the Department for
Furthermore, we evaluate the population structure of all 32 managed marine fish Marine Research,
species in the north-east Atlantic and relate this structure to current management Senckenberg Insti-
tute, Südstrand 40,
units and practice. Although a large number of studies on genetic population
26382 Wilhelm-
structure have been published in the last decades, data are still rare for most exploited shaven, Germany.
species. The mismatch between genetic population structure and the current Tel.: +49 4421 9475
management units found for six species (Gadus morhua, Melanogrammus aeglefinus, 253
Merlangius merlangus, Micromesistius poutassou, Merluccius merluccius and Clupea Fax: +49 4421 9475
222
harengus), emphasizes the need for a revision of these units and questions the
E-mail: henning.reiss
appropriateness of current management measures. The implementation of complex @senckenberg.de
and dynamic population structures into novel and less static management procedures
Received 13 February
should be a primary task for future fisheries management approaches. 2008
Accepted 23 December
Keywords Cod, fish stocks, fisheries management, herring, north-east Atlantic, 2008
sustainability
Introduction 362
Determination of populations and management units 363
Mismatch between management and biological units in the NE Atlantic 371
Fisheries management and management units in the NE Atlantic 371
Population structure of demersal fish species 372
Cod 372
Haddock 378
Other demersal roundfish species 378
Plaice 379
Sole 379
Other flatfish species 380
2009 Blackwell Publishing Ltd DOI: 10.1111/j.1467-2979.2008.00324.x 361

Genetic structure and management: mismatch H Reiss et al.
Redfish 380
Rays and skates 381
Pelagic fish species 381
Herring 381
Capelin 382
Blue whiting 382
Other pelagic species 383
Spatial mismatch – implications for fisheries management 383
Acknowledgements 385
References 385
management boundaries (Halliday and Pinhorn

Introduction
1990). Ignoring the congruence of spatial scales
One of the primary objectives of fisheries manag- between population structure of fish species and
ers is to ensure sustainability in harvesting fish management units can result in reduced productivity
stocks and to avoid a depletion of these stocks. and local reduction of populations (Kenchington
The severe decline of many commercial fish stocks 2003; Hughes and Stachowicz 2004; Reusch et al.
in the last decades, however, and the slow or 2005; Worm et al. 2006). In the most extreme case,
even failed recovery of some overexploited stocks depleted or extinct local populations will not be
raise the question whether current management replaced by immigrants or recruits from other pop-
strategies are sufficient for a sustainable use of ulations, which in turn might have a negative effect
marine resources (e.g. Hutchings 2000; Myers not only on local fish populations, but also on total
and Worm 2003; Daw and Gray 2005; Worm recruitment and fisheries yields (ICES, 2006). In an
et al. 2006). One prerequisite for sustainable aggregated management in which a population
management is the matching of biological pro- complex is managed as a single population, extinc-
cesses and management action. However, mis- tion of subpopulations would be possible before the
matches between the ecology or biology and the analyses of aggregated data would indicate a popu-
realized management action frequently occur, lation decline (Frank and Brickman 2000). Indeed,
since managers need to include a variety of partly simulations for cod populations, using a population
conflicting factors in their management strategy, dynamics model, showed that the combined man-
such as biological, economic, social or even agement of two subpopulations as one unit resulted
political factors. Such mismatches often remain in an over-fishing of the more vulnerable subpopu-
even when highlighted as problematic as the lation (Fu and Fanning 2004; Sterner 2007).
management system is slow to adapt and political Furthermore, overexploited fish populations can
inertia often reduces flexibility. undergo a loss of genetic diversity (Hauser et al.
In fisheries management and assessment, fish 2002), and with it the ability for the species to adapt
stocks or populations are the fundamental biological and evolve to new environmental circumstances
unit, but the choice of spatial management areas does (Mace and Purvis 2008). The recent findings of
not necessarily delineate biological meaningful enti- species distribution shifts and failure in recruitment
ties (Carvalho and Hauser 1994; Waples and Gag- as a response to climatic changes (O’Brien et al. 2000;
giotti 2006). For example, fisheries management Rose 2005b; Rindorf and Lewy 2006; Hannesson
areas in the north-west (NW) Atlantic were originally 2007) emphasizes the importance of maintaining the
delimited based on species and fishery distribution, adaptive capability of exploited fish populations.
oceanographic features, political and administrative The potential of genetic data to improve the
boundaries, and homogeneity of fisheries participa- understanding of population structure, along with
tion, whereas only the population structure of the intraspecific diversity, and consequently the devel-
most important target species, cod (Gadus morhua, opment of specific management strategies is well
Gadidae) and haddock (Melanogrammus aeglefinus, described for freshwater and anadromous fish spe-
Gadidae), were considered for the determination of cies (e.g. Carlsson et al. 1999; Shaklee et al. 1999;
362 2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

Beacham et al. 2002, 2004). The natal homing management and assessment tools are mainly based
behaviour, and in consequence, the reproductive on the ecological criteria of populations, the corre-
isolation of many anadromous fish species results in sponding management aims such as the sustain-
many genetically distinct populations. Though in ability of spawning stock biomass and the
marine species the opposite seems to be the case, conservation of genetic diversity are predominantly
typically exhibiting low genetic population differen- linked to the evolutionary criteria of populations.
tiation for many species (Ward et al. 1994), recent Such discrepancy between management tools and
studies have revealed genetic structuring among aims emphasizes the need for integrating genetic
populations that were previously thought to exhibit data of population structure into fisheries manage-
homogeneous population structure. That holds true ment strategies.
even for highly mobile species with a wide spatial A key question for the application of genetic
distribution and high dispersal potential (Jørstad methods to fisheries management is to assess the
et al. 1991; Hutchinson et al. 2001). Thus, fisheries level of divergent populations that is required to
managers are confronted with sometimes complex justify their separate management (Waples et al.
and dynamic population structures, but the estab- 2008). Such consideration depends upon biological
lished management tools and spatial management characteristics and the population history of the
units remain rather static. species, as well as the underlying management and
Although a large amount of literature about conservation objectives (Palsbøll et al. 2007). The
genetic population structure of marine fish species methodological aspects of determining population
exists (reviewed by e.g. Carvalho and Hauser 1998; structure by using genetics are beyond the scope of
Shaklee and Bentzen 1998; Ruzzante et al. 1999; this review, and more detailed information on
Ward 2002; O’Leary et al. 2007), few studies have genetic markers and methods can be found in
specifically addressed the intersection between fish- Carvalho and Hauser (1998), Parker et al. (1998),
eries management and population genetics (Ryman Ward (2000), Kalinowski (2005) and Hauser and
and Utter 1987; Ward 2000; Smedbol and Seeb (2008). Various threshold levels of gene flow
Stephenson 2001; Kenchington et al. 2003; Laikre have been proposed to define a population and/or a
et al. 2005; Waples et al. 2008). Thus, the main management unit, a key criterion being demo-
objectives here are (i) to compile and discuss key graphic independence of populations (Waples and
aspects related to the identification of biological Gaggiotti 2006; Palsbøll et al. 2007). For opera-
units or populations for fisheries management based tional reasons we have used the criteria of Bentzen
on genetic methods and (ii) to evaluate the genetic (1998): if a significant and reproducible genetic
population structure of all managed fish species in differentiation can be detected, the populations
the north-east (NE) Atlantic and relate this struc- should be considered demographically independent.
ture to current management units and practice. The Waples and Gaggiotti (2006) argued that if an
term ‘stock’ is only used whenever it refers to adequate number of highly variable markers are
fisheries management entities, otherwise the term used, it may be possible to detect population
population is preferred. differentiation when the migration rates are higher
than the level required for demographic indepen-
dence. However, as the vast majority of fish
Determination of populations and
population genetic papers rely on a small number
management units
of markers (Table 1), the practical advantage of the
The biological concept of population is crucial to departure form panmixia criteria outweigh its
both ecology and evolutionary biology, and despite potential drawbacks. Furthermore, against the
the variety of definitions available, they mostly fall background of precautionary principles, a spatial
under two major types of definitions, reflecting the separation of management and assessment units on
dichotomy between ecology and evolutionary a smaller scale than the ‘real’ spatial population
biology. The ecological definition reflects mainly structure would be less detrimental than the con-
the co-occurrence and demographic interaction of verse scenario. Indeed, such error would result in
individuals in space and time, whereas evolutionary inflated management procedures beyond require-
criteria are based on genetic structure due to ments, and would have significant economic than
reproductive interactions among individuals ecological consequences. The somewhat conflicting
(Waples and Gaggiotti 2006). While fisheries conclusions of different genetic studies presented
2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395 363

Table 1 Genetic population structure studies in managed marine fish species in the NE Atlantic.
364
Evaluation
Species Region Location details (no. sites) Diff. Mis. Markers (no. loci) size/rep/mark Source
Cod Entire Atlantic NS (6), IS (1), CSs (2), Channel (2), Yes Yes msats (5) +/)/s Hutchinson et al. (2001)
BS (1), Scot (1)
Entire Atlantic Newf (5), Nov (1), Labrador (2), BS (1) Yes Yes msats (6) +/+/s Bentzen et al. (1996)
Entire Atlantic Norw n (1), IS (1), Nov (1), Newf (1) Yes No minisats (1) s/)/) Galvin et al. (1995)
entire Atlantic Baltic (1), BS (1), Ice (3); Greenl (3), Yes No msats (6) s/)/s O’Leary et al. (2007)
Scot (1)
Entire Atlantic NS (1), Newf (1) No No mtDNA (1) )/)/s Smith et al. (1989)
Entire Atlantic Ice (1), NS (1), BS (2), Nov (1), Yes No scnDNA (11) +/)/+ s? Pogson et al. (1995)
Newf (1)
Entire Atlantic Scot (2), BS (1), Trondheimfjord (1), Yes No scnDNA (6) s/)/s s? Jónsdóttir et al. (2003)
CS (1), NS (4), Ice (1)
Entire Atlantic Newf (4), Nov (4), Ice (1), NS (1) Yes No scnDNA (10) +/)/+ s? Pogson (2001)
Balsfjord (1), BS (1)
Entire Atlantic NS (1), Greenl (1), Nov (1), Ice (1), BS No No allozyme (13) +/)/s s? Mork et al. (1985)
(1) Norw (2), Baltic (2)

NE Atlantic Skagerrak (5) Yes Yes msats (13) +/)/+ Jorde et al. (2007)
NE Atlantic Norw (11), BS (1), Sptz (1) Yes Yes msats (10), scnDNA (1) +/+/+ s Westgaard and Fevolden (2007)
NE Atlantic Faroe (5), NS (2), Baltic (2) Yes No msats (9), scnDNA (1) +/+/+ s Nielsen et al. (2007)
NE Atlantic Baltic (1), NS (1) Yes No msats (9) +/+/s Poulsen et al. (2006)
NE Atlantic Norw (8) Yes Yes msats (6), scnDNA (1), +/+/+ s Wennevik et al. (2008)
allozymeH (6)
NE Atlantic Ice (5), Faroe (2) Yes No msats (9), scnDNA (1) +/+/+ s Pampoulie et al. (2008)
NE Atlantic Ice (22) Yes Yes msats (9), scnDNA (1) +/+/+ s Pampoulie et al. (2006)
NE Atlantic Skagerrak (6) Yes Yes msats (10) +/)/+ Knutsen et al. (2003)
NE Atlantic Baltic (12), NS (2) Yes No msats (9) +/+/s Nielsen et al. (2003)
NE Atlantic NS (1), Baltic (1), BS (1) Yes No msats (9) +/+/s Nielsen et al. (2001)
NE Atlantic NS (1), Norw and BS (10), Sptz (1) Yes Yes msats (7), scnDNA (1) +/+/+ s Skarstein et al. (2007)
NE Atlantic Greenl (9), Ice (42) No No mtDNA (1) )/+/s Árnason et al. (2000)
NE Atlantic Faroe (5) No No mtDNA (1) )/)/s Sigurgı́slason and Árnason (2003)
NE Atlantic Norw n (5), Norw s (2), BS (2) No No mtDNA (1) )/)/s Árnason and Pálsson (1996)
NE Atlantic Norw (6) and BS (3) Yes Yes mtDNA (1) )/)/s Dahle (1991)
NE Atlantic Ice (12) No No mtDNA (1) )/+/s Árnason et al. (1992)
NE Atlantic NS (6), Ice (8), CS (3), Baltic (1), Yes No scnDNA (1) +/+/) s Case et al. (2005)
BS (2), Norw (2)
2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

Table 1 Continued.
Evaluation
NE Atlantic Ice (2) Yes Yes scnDNA (1) +/+/) s Jónsdóttir et al.
(2002)
Cod NE Atlantic Ice (6) Yes Yes scnDNA (1); +/)/) s Jónsdóttir et al. (1999)
allozymeH (1)
NE Atlantic Ice (5) Yes Yes scnDNA (5) s/)/s s? Imsland et al. (2004)
NE Atlantic Norw n (8) Yes Yes scnDNA (1) +/)/) s Pogson and Fevolden (2003)
NE Atlantic Norw n (22) Yes Yes scnDNA (1) s/+/) s Fevolden and Pogson (1997)
NE Atlantic Ullsfjord (7) Yes Yes scnDNA (1) +/+/) s Sarvas and Fevolden (2005b)
NE Atlantic Ice (2) Yes Yes scnDNA (1), +/+/) s Jónsdóttir et al. (2001)
allozymeH (1)
NE Atlantic Norw (35), BS (5), Sptz (5), Yes Yes scnDNA (1) +/+/) s Sarvas and Fevolden (2005a)
NS (1)
NE Atlantic Norw s (3), Norw n (2) Yes Yes scnDNA (1) +/)/) s Berg et al. (2005)
NE Atlantic BS (1), Norw (5) Yes No allozymeH (1) +/+/) s? Dahle and Jørstad (1993)
NE Atlantic Skagerrak (4) No No allozymeH (6) +/+/) s? Gjøsæter et al. (1992)

NE Atlantic Norw (8) Yes Yes allozymeH (1) +/+/) s? Nordeide (1998)
NE Atlantic Norw (8) No No allozyme (6) +/)/) s? Mork and Giæver (1999)
NE Atlantic Norw (28) Yes Yes allozyme (6) +/+/) s? Jørstad and Nævdal (1989)
NE Atlantic Norw (3) Yes Yes allozyme (6), +/)/+ s Dahle et al. (2006)
msats (10),
scnDNA (1)
NE Atlantic Norw (7), Danish Belt Sea (2) Yes Yes allozymeH (1) +/)/) s? Husebø et al. (2004)
NW Atlantic Newf (1), Grand Bank (1) Yes Yes msats (5) +/+/s Ruzzante et al. (1997)
NW Atlantic Newf (10), Nov (6), Labrador (3) Yes Yes msats (5) +/+/s Ruzzante et al. (1998)
NW Atlantic Nantucket Shoals (1), Georges Yes Yes msats (5), +/+/+ s Lage et al. (2004)
Bank (1), Browns Bank (1) scnDNA (1)
NW Atlantic NW Atlantic (19) Yes No msats (7), +/+/+ s Beacham et al. (2002)
scnDNA (1)
NW Atlantic Newf (6), Grand Bank (3) Yes Yes msats (5) s/+/s Ruzzante et al. (1996)
NW Atlantic Newf (10) and Trinity Bay (3), Yes Yes msats (5) +/+/s Ruzzante et al. (2000a)
Labrador Gilbert Bay (4)
NW Atlantic Newf (5) No No mtDNA (1) s/)/s Carr et al. (1995)
NW Atlantic Grand Banks (10) No No mtDNA (1) )/+/s Pepin and Carr (1993)
365
Table 1 Continued.
366
Evaluation
Haddock Entire Atlantic Georges Bank (1), Nanetucket Yes Yes msats (4) +/+/) Lage et al. (2001)
Shoals (1), Nov (2), Norway (1)
NE Atlantic NS (3), Norw (33), Ice (1), No No allozyme (8) +/+/) s? Giæver and Forthun (1999)
Skagerrak (1)
NE Atlantic NS (35), Faroe (12), Rockall (8), Yes Yes allozyme (1) +/+/) s? Jamieson and Birley (1989)
Scot (4)
NW Atlantic Newf (1), Nov (4) No No mtDNA (1) )/+/s Zwanenburg et al. (1992)
Hake NE Atlantic and Med Med (2), CS (1), NS (1), BB (1), Yes Yes msats (6) +/)/s Lundy et al. (1999)
Port (1)
NE Atlantic and Med Med (1), Port (3), BB (4) Yes No msats (5) s/)/s Castillo et al. (2005)
NE Atlantic and Med BB (7), Norw (1), Med (1) Yes No msats (5), +/+/+ Lundy et al. (2000)
mtDNA (3)
NE Atlantic and Med Med (11), CS (1), BB (1), Atlantic (2) Yes No allozyme (19) +/+/s s? Cimmaruta et al. (2005)
NE Atlantic and Med Med (4), NE Atlantic (5) Yes No allozyme (21) +/)/s Roldán et al. (1998)
NE Atlantic and Med Med (8), NS (1) Yes No allozyme (5), s/)/+ Lo Brutto et al. (2004)
mtDNA (1)
NE Atlantic and Med Port (1), Med (1) Yes No allozyme s/)/) s? Imsiridou and Triantaphyllidis (2001)
Whiting NE Atlantic NS (2), IS (1), Baltic (1) Norw n (1) No No msats (3) +/)/) Rico et al. (1997)
NE Atlantic NS (4), IS (3), Hebrides (1), BB (1) Yes Yes msats (7) s/)/s Charrier et al. (2007)
Pollack NE Atlantic Bretagne (3), Channel (1), No No msats (6) s/)/s Charrier et al. (2006b)
BB (1), Norw (1)
Saithe No information
Plaice NE Atlantic NS (3), Ice (1), Shetland (1), (Yes No msats (6) s/+/s Hoarau et al. (2002)
Norw (2), BB (1), IS (2)
NE Atlantic IS (6), NS (2) No No msats (8) )/)/s Watts et al. (2004)
NE Atlantic NS (3), Ice (1), Shetland (1), Yes No mtDNA (1) s/+/s Hoarau et al. (2004)
Norw (2), BB (1), IS (2)
Sole NE Atlantic French Atlantic coast (9), Med (17) Yes No allozyme (12) s/+/s s? Kotoulas et al. (1995a)
NE Atlantic IS (3), NS (2), BB (1) Yes No DNA RAPD )/)/) Exadactylos et al. (2003)
NE Atlantic and Med Med (4), BB (9), Channel (1), Baltic (1) Yes No scnDNA (3) s/+/) s? Rolland et al. (2007)
NE Atlantic and Med NS (2), IS (3), BB (1), Med (1) Yes No allozyme (27) s/)/s s? Exadactylos et al. (1998)
Greenland halibut Entire Atlantic Faroe (1), BS (2), Norw (1), Greenl (2), Yes Yes msats (9) +/)/s Knutsen et al. (2007)
Canada (1)

Table 1 Continued.
Evaluation
Entire Atlantic NW Atlantic (4), No No mtDNA (1) s/)/s Vis et al. (1997)
Gulf of St. Lawrence (1),
Ice (1), Norw (1)
Entire Atlantic Greenl (2), Jan Mayen (1), No No allozyme (3) +/)/) s? Igland and Nævdal
BS (1), Faeroe (1), Shet (1) (2001)
NW Atlantic NW Atlantic (3), Gulf of St. Yes No allozyme (2) +/)/) s? Fairbairn (1981)
Lawrence (1), Bering Sea (1)
Turbot NE Atlantic Cantabric Sea (1), NW Spain (1) No No msats (12), s/)/+ Bouza et al. (2002)
allozyme (17)
NE Atlantic Baltic (9) No No msats (8) s/+/s Florin and Höglund (2007)
NE Atlantic Irish (1), Norw (1) No No msats (3) s/)/) Coughlan et al. (1998)
NE Atlantic BB (1), NS (1), Baltic Sea (6) Yes No msats (8) s/+/s Nielsen et al. (2004)
NE Atlantic Cantabric coast (1), Atlantic (2) No No allozyme (14) s/)/s s? Bouza et al. (1997)
NE Atlantic and Med Kattegat (1), NS (2), Channel (1), Yes No allozyme (6) )/)/) s? Blanquer et al. (1992)
Port (1), Med (3), Marocco (1)

Megrim NE Atlantic and Med BB (2), Channel (2), CS (1), Yes No mtDNA (1), rDNA (1) +/)/+ Garcia-Vazquez et al. (2006)
Scot (1), Port (1)
European flounder NE Atlantic NS (4), Baltic (5), Faroe (1), Yes No msats (9) s/+/s Hemmer-Hansen et al. (2007)
Norw (2), BB (1), IS (1)
NE Atlantic Channel (2), CS (1), Baltic (5), Yes No allozyme (17) s/)/s s? Galleguillos and Ward (1982)
Med (2)
NE Atlantic and Med NS (4), Baltic (3), BB (2), Port (5), Yes No allozyme (8) s/)/) s? Borsa et al. (1997)
Med (4)
Brill NE Atlantic and Med Kattegat (1), NS (1), Channel (1), No No allozyme (10) )/)/s s? Blanquer et al. (1992)
Port (1), Med (2)
Lemon sole No information
Witch flounder No information
Dab No information
Anglerfish NE Atlantic IS (4), Scot (1) Yes No allozyme (11) s/)/s s? Crozier (1987)
NE Atlantic and Med BB (4), IS and CS (4), Hebrides No No mtDNA (1) s/+/s Charrier et al. (2006a)
and NS (4)
Norway pout No information
Sandeel NE Atlantic NS (7), BS (1) No No allozyme (3) +/+/) s? Nævdal and Thorkildsen (2002)
367
368
Table 1 Continued.
Evaluation
Thornback ray NE Atlantic Channel (4), NS (6), IS (4) Yes No msats (5) s/+/s Chevolot et al. 2006a)
NE Atlantic and Med BB (3), Med (2), Azores (5), IS (2), Yes No mtDNA (1), msats (5) )/+/+ Chevolot et al. (2006b)
NS (3), Channel (2)
Thorny skate Entire Atlantic Newf (1), Ice (8), NS (2), Kattegat (1) Yes No mtDNA (1) s/+/s Chevolot et al. (2007)
Beaked redfish Entire Atlantic NW Atlantic (14), Faroe (1), Ice (2), Yes No msats (8) s/)/s Roques et al. (2002)
Greenl (2), Norw (2)
Entire Atlantic Irminger Sea (34), Ice (3), Norw (2), Yes No allozyme (3) s/+/) s? Johansen et al. (2000b)
Canada (2)
Acadian redfish NE Atlantic Norw (5), Ice (1) Yes No allozyme (2) +/+/) s? Johansen et al. (2002)
Golden redfish NE Atlantic Ice (7), Greenl (4), Reykjanes Ridge (5) Yes No allozymeH (3) s/+/) s? Johansen et al. (2000a)
NE Atlantic Ice (8), Greenl (2) Yes No allozymeH (3) +/+/) s? Nedreaas et al. (1994)
Atlantic herring Entire Atlantic CS (1), Ice (1), Baltic Sea (1), Nov (7) Yes No msats (9) +/+/s McPherson et al. (2004)
Entire Atlantic NW Atlantic (3), IS and CS (6), Baltic (8), Yes Yes allozyme (6) +/)/) s? Jørstad et al. (1991)
NS and Norw (8), Norw n (3)
NE Atlantic NS (10) Yes Yes msats (9) +/+/s Mariani et al. (2005)
NE Atlantic Baltic (3), Channel (1), NS (1), Scot (1), Yes Yes msats (9) +/+/s Bekkevold et al. (2007)
Norw (1)
NE Atlantic NS (4) Yes Yes msats (4) s/)/) Shaw et al. (1999)
NE Atlantic NS (4), Scot (2), Skagerrak (18), Yes No msats (9) +/+/s Ruzzante et al. (2006)
Channel (1), Norw s (2), Shetlands (9)
NE Atlantic NS (2), Skagerrak (3), Kattegat (4) Yes No msats (9) +/+/s Bekkevold et al. (2005)
NE Atlantic Baltic (10) Yes No msats (9) +/+/s Jørgensen et al. (2005a)
NE Atlantic Ice (2), NS (2), CS (1), Baltic (1), Norw (4) Yes No mtDNA (2) s/+/s Hauser et al. (2001)
NE Atlantic NS (4), Skagerrak and Kattegat (3) No No mtDNA (1) s/)/s Dahle and Eriksen (1990)
NE Atlantic Ice (1), NS (1), Norw (2) Yes Yes mtDNA (1), allozyme (13) s/)/+ s? Turan et al. (1998)
NE Atlantic Norw (2) Yes Yes mtDNA (1), allozyme (6) )/)/+ s? Jørstad et al. (1994)
NE Atlantic IS and CS (9), Baltic Sea (1) No No allozyme (5) +/+/) s? King et al. (1987)
NE Atlantic NS (2), Skagerrak (7), Kattegat (1), Baltic (4) No No allozyme (13) +/+/s s? Ryman et al. (1984)
NW Atlantic Nov (5) Yes No msats (9) +/)/s McPherson et al. (2001)
NW Atlantic Nov (4) No No msats (9) +/+/s McPherson et al. (2003)
NW Atlantic Nov (1), Nanetucket Shoals (1) No No allozyme (4) +/+/) s? Safford and Booke (1992)
NW Atlantic Gulf of Maine and of St. Lawrence (7) No No allozyme (5) +/+/) s? Kornfeld et al. (1982)

Table 1 Continued.
Evaluation
Capelin Entire Atlantic Norw (2), BS (1) Yes No msats (11) s/+/+ Røed et al. (2003)
Entire Atlantic NW Atlantic (7), Yes No mtDNA (1) s/)/s Dodson et al. (1991)
Ice (1), BS (1)
Entire Atlantic Newf (1), BS (1) Yes No mtDNA (1) )/+/s Birt et al. (1995)
NE Atlantic Greenl (3) Yes Yes allozyme (4) +/)/) s? Sørensen and
Simonsen (1988)
NE Atlantic Balsfjord (1), BS (1) No No allozyme (4) +/)/) s? Mork and Friis-Sørensen
(1983)
Blue whiting NE Atlantic Hebrides and CS (6), Ice (1), Yes No msats (6) +/+/s Ryan et al. (2005)
Norw (2), Port (1), Mediter. (1)
NE Atlantic BB (1), Hebrides (1), CS (1), Yes Yes msats (5) s/+/s Was et al. (2008)
Rockall (2), Porcupine Bank (2)
NE Atlantic British Islands (1) No No allozyme (3) +/)/) s? Mork and Giæver (1995)
NE Atlantic CS and Hebrides (9), Norw (52), Yes No allozyme (2) +/+/) s? Giæver and Stien (1998)

Ice (1), BB (1) Med (2)
Mackerel Entire Atlantic NS (1), Med (1), NE Atlantic (2), Yes No mtDNA (2) s/+/s Nesbø et al. (2000)
NW Atlantic (1)
Entire Atlantic NW (1) and NE Atlantic (1) Yes No mtDNA (1) )/)/s Scoles et al. (1998)
NE Atlantic and Med Atlantic (4), Med (6) Yes No mtDNA (1) s/)/s Zardoya et al. (2004)
Horse mackerel NE Atlantic and Med NS (1), IS (1) BB (2), Port (1), No No msats (4) +/+/) Kasapidis and Magoulas (2008)
Med (5), Mauretania (1)
NE Atlantic and Med NS (2), BB (2), Channel (1), No No mtDNA (1) s/)/s Karaiskou et al. (2004)
Atlantic (1), Med (4)
NE Atlantic and Med Med (4), Port (3), BB (2) No No mtDNA (1) s/)/s Comesana et al. (2008)
NE Atlantic and Med NS (1), BB (1), west of Britain (1), No No allozyme (1) +/)/) s? Borges et al. (1993)
Port
NE Atlantic and Med Med (9), Port (3), BB (3), NS No No allozyme (12) +/+/s s? Cimmaruta et al. (2008)
(2), Ireland (2)
Anchovy NE Atlantic and Med Atlantic (5), Med (13), Black Yes No mtDNA (1) s/+/s Magoulas et al. (2006)
Sea (4), BB (2)
Sprat No information
Swordfish Global Pacific (6), Atlantic (3), Med (1) Yes No mtDNA (1) )/+/s Rosel and Block (1996)
369
Table 1 Continued.
370
Evaluation
Global Pacific (6), Atlantic (3), Med (1), Yes No mtDNA (1) )/)/s Chow et al. (1997)
Indian Ocean (2)
Global Pacific (1), Atlantic (4), Med (1), Yes No mtDNA (1) s/+/s Chow and Takeyama
Indian Ocean (1), Tarifa (1) (2000)
Global Pacific (1), NW Atlantic (1), S Yes No mtDNA (1) s/)/s Alvarado Bremer et al.
Atlantic (1), Med (1) (1996)
NE Atlantic Med (3), Gulf of Guinea (1) Tarifa (1) Yes No mtDNA (1) s/)/s Kotoulas et al. (1995b)
and Med
NE Atlantic Med (9), Strait of Gibraltar (1) No No allozyme (2) s/+/) s? Pujolar et al. (2002)
and Med
NW Atlantic NW Atlantic (2), S Atlantic (2) Yes No mtDNA (1) )/+/s Alvarado Bremer et al.
and S Atlantic (2005)
Bluefin tuna Entire Atlantic and Med Med (16), NE Atlantic (1), NW No No allozyme (13) s/+/s s? Pujolar et al. (2003)
Atlantic (1)
Bluefin tuna NE Atlantic NW Atlantic (1), Gulf of Mexico (1), Yes No msats (6) )/)/s Broughton and Gold (1997)
Med (2)
NE Atlantic and Med Med (8), NE Atlantic (1), NW No No mtDNA (1) s/+/s Alvarado Bremer et al. (2005)
Atlantic (1)
NW Atlantic and Med NW Atlantic (1), Med (1) No No mtDNA (1), s/)/+ s? Ely et al. (2002)
scnDNA (1)
Tusk Entire Atlantic Davis and Denmark Strait (2), Yes No allozyme (8) +/)/) s? Johansen and Nævdal (1995)
Faroe (1),
Rockall (1), Norw (4), Scot (2)
Roundnose No information
grenadier
Ling No information
Blue ling No information
Diff. = differentiation among population on the studied scale; Mis. = indications for a mismatch with management units. Evaluation criteria: sample size (size): <20 individuals ()), 20–49 (s), ‡50 (+);
markers (mark): msats < 5 loci ()); 5–9 loci (s); ‡10 loci (+); mtDNA (s); scnDNA < 5 loci ()); 5–9 loci (s); ‡10 loci (+); allozymes < 10 polymorphic loci ()), ‡10 loci (s); combination of different markers
(+), Hallozymes including haemoglobin; temporal replication (rep): (sampling in different years at least at one location or sampling of different age groups): yes (+), no ()); selectivity: at least one locus
under selection (s) or possibly under selection (s?). Locations: BB = Bay of Biscay; Port = Portuguese coast; Med = Mediterranean; NS = North Sea; CS = Celtic Sea; IS = Irish Sea; BS = Barents Sea;
Ice = Iceland; Norw s/n = Norwegian coast, north and south; Scot = Scotian Shelf; Sptz = Spitzbergen; Shet = Shetlands; Greenl = Greenland; Nov = Nova Scotia; Newf = Newfoundland.

here may reflect the difficulties involved in deter- It is important to be aware that genetic data are
mining the genetic structure of marine fish that only one component of defining biological units,
typically display high gene flow. Indeed the genetic and other phenotypic markers and criteria should
differentiation among populations of marine fish is ideally be incorporated in the assessment of biolog-
generally characterized by a low signal:noise ratio ically meaningful management units (see e.g.
(Waples 1998). In this regard, three factors appear McQuinn 1997). Nevertheless, genetic population
to be essential to maximize the power to detect structure should be regarded as a minimum
structure in marine fishes: temporal replication, a prerequisite for the definition of these units, since
sufficient sample size, and the use of adequate genetic data provide a rather conservative measure
molecular markers (Waples 1998). Although other of population differentiation.
factors may be important (e.g. sampling design, life
stage sampled, etc.), these criteria were used in a
Mismatch between management and
qualitative evaluation of the fish population genetics
biological units in the NE Atlantic
literature (see Table 1).
To be useful in the context of management, In order to evaluate the genetic population struc-
temporal stability of genetic population structure is ture of fish species in the NE Atlantic and the
of major importance, as genetic composition may mismatches with the present management units, we
vary as much over time at a single location as over summarize current knowledge about population
large distances (e.g. Small et al. 2005; Florin and structure. The landings data for each species were
Höglund 2007; Klanten et al. 2007). Such variance extracted from the Eurostat/ICES database on catch
may arise from high variability in reproductive statistics by using the FAO-FishStat Plus software
success of adults resulting in year-classes compris- (FAO, 2006).
ing the progeny of a small proportion of the
spawning population only (Hedgecock 1994;
Fisheries management and management units
sweepstakes hypothesis), as shown in marine inver-
in the NE Atlantic
tebrates (David et al. 1997; Hedgecock et al. 2007).
Alternatively, the inclusion of genetically distinct Fisheries management in the NE Atlantic is now
populations at one location, which are temporally mostly based on the European union (EU) Common
separated within a spawning season (McPherson Fisheries Policy (CFP), which came into force in
et al. 2003; Jørgensen et al. 2005b), may prove 1982 and was last reformed in 2003 (EC 2003).
misleading if sampling was undertaken over a Fisheries outside EU waters are managed by inter-
longer time span. The inclusion of unknown or national agreements which can be bi-lateral, such
feeding aggregations rather than spawning compo- as those between the EU and Norway in the North
nents into analysis of genetic structuring, can Sea and the EU and Russia in the Baltic Sea, or
further lead to misleading estimates of genetic between more parties, such as coastal states nego-
differentiation. tiations or by international Commissions such
Estimates of demographic properties using popu- as the North East Atlantic Fisheries Commission
lation genetic data rely on the assumption of marker (NEAFC see below). The main instrument for
neutrality and that allele frequencies respond pri- managing fish stocks is stock-specific annual total
marily to mutation, drift and gene flow. Neverthe- allowable catches (TACs) supplemented by technical
less, for recently differentiated populations with measures such as mesh sizes, effort control such as
large effective population size, selected markers may ‘days at sea’, gear and by-catch restrictions and to a
detect population differentiation more precisely than lesser extent spatial and temporal closures of specific
neutral markers due to a more rapidly changing areas (see Dankel et al. 2008). Such management
allele frequencies. A significant drawback of using measures are used based on the evidence provided
these markers is the unknown strength of selection by scientific assessment of stock status and dynam-
(Sotka and Palumbi 2006). Nevertheless, as mark- ics, carried out by the International Council for the
ers under selection reflect processes of natural Exploration of the Sea (ICES) Advisory Committee
selection rather than reproductive relationships, and associated Working Groups. Whilst the current
they could be particularly important for preserva- review focuses on the mismatch between population
tion of local adaptations (Conover et al. 2006; structure and management units, there is often
Hauser and Carvalho 2008). already a mismatch between scientifically assessed

units and the management unit (e.g. horse mechanism for adjusting stock definitions is not
mackerel in the North Sea, until recently herring based on peer reviewed publications, but usually on
in the western Baltic Sea; Table 2). The spatial ‘grey evidence’ which is submitted to the ICES
management units differ from species to species but internal review process. The process is not systematic
the main units in the NE Atlantic are the ICES and sometimes managers do not accept ICES advice.
divisions and subdivisions shown in Fig. 1. There is also a lack of clarity in some stocks in the way
On the broad scale, these management units are that advice is implemented. For example, stock
associated with collection areas for fishery statistics. assessment is carried out on a specific spatial resolu-
Thus, they were geo-economic in nature and not tion, but then the regulatory authorities combine
developed in relation to population integrity, but the advice to quotas at higher resolution. Thus, the
rather for collection of fisheries data. The initial ICES mismatch is not just the management areas with the
areas were set up in 1904 (for the fisheries statistics biological structure of fish populations, but there is
for 1903), with originally 20 areas (I–XX) covering also often in each direction a mismatch with the
the entire North Atlantic north of 36 N (Hans assessment advice based on ICES stocks (see Table 2).
Lassen, personal communication, ICES). As various In the NE Atlantic, 32 marine fish species or
international treaties were drawn up, the geo- species groups are managed by annual TACs within
graphic expanse of these areas changed with their specific management areas. Current knowledge on
management. The western Atlantic was taken out genetic population structure is summarized in
of the ICES system in 1950 when the International Table 1. Despite limited available information for
Commission for the Northwest Atlantic Fisheries the majority of species and even lacking information
(ICNAF) was established by Canada and the USA. In for nine species, indications for a mismatch between
1979 with the extension of Exclusive Economic population structure and current management
Zones (EEZ), ICNAF was replaced by the Northwest units were found for cod (G. morhua), haddock
Atlantic Fisheries Organization and lead to the (M. aeglefinus), whiting (Merlangius merlangus),
current system in the NW Atlantic (Halliday and European hake (Merluccius merluccius), herring
Pinhorn 1990). In the remaining North Atlantic, (Clupea harengus) and blue whiting (Micromesistius
the Permanent Commission formed in 1946, devel- poutassou) (Table 2; Fig. 2). Nevertheless, it has to
oped into the NEAFC in 1959, which was then be mentioned here that the variability in the quality
reformed in 1980 with the extensions of the of genetic data presented was relatively high
national fishing limits to 200 nautical miles of the depending on the sample size, sampling of spawning
EEZ. As the EU enlarged, it took increasingly more or feeding individuals, temporal replication, number
fishing areas into the CFP. Although there is some of polymorphic loci and selectivity of markers.
flexibility based on new information to the ICES Although a quality assessment was carried out
boundaries, the ICES areas, which were determined based on sample size, temporal replication and
by socio-economic criteria, are rarely adjusted to fit characteristics of markers, we can only provide a
the biology of stocks. There is also no comprehen- subjective indication of the reliability of the patterns
sive documentation for amendments to ICES areas. described (Table 1), though multi-species data do
The description of management units and organi- provide a framework for comparative analyses.
zations suggests that the management units are very
fixed and do not in any way reflect the underlying
Population structure of demersal fish species
structure of the fished populations. However, the ICES
system does allow data from areas to be merged or Cod
split based on the biology of fish. ICES provide advice The Atlantic cod (G. morhua, Gadidae) is one of
for fish ‘stocks’. However, the definition of a stock the most important commercial fish species within
varies: it is based on the best available knowledge its distribution range throughout the boreal region
at the time. As new knowledge on population of the North Atlantic. In the NE Atlantic 35% of
structure (demographic, morphometric or genetic) the 2.23 million tons of demersal fish landed in
was brought to ICES, working groups have consid- 2005 was cod (803 000 tons). The main fishing
ered provided recommendations to merge stocks or fleets targeting cod in the NE Atlantic are those of
split stocks. An example is the history of the Norway and Iceland, but cod is a by-catch species
management units of herring around Ireland (see in almost all demersal and some pelagic fisheries
Molloy 2006). It is important to note that the in the area. However, since the 1970s landings

Table 2 Mismatch between management and assessment areas (see Fig. 1) as well as between management areas and
genetic structure based on the evaluation shown in Table 1.
Management Mismatch with Mismatch with genetic

Species areas assessment areas Stock status/trend structure
Cod I, II1 NEAC Full reproductive capacity, Differentiation between

risk of overexploitation NEAC and NCC (very likely)
NCC Reduced reproductive Microgeographical
capacity, historical low differences between fjords
(possible)
IIa2, IV IV, Skagerrak, Risk of reduced reproductive 3–4 distinct populations in
VIId capacity area IV (possible)
22–242 – Risk of reduced reproductive
capacity
25–322 – Risk of reduced reproductive
capacity
Skagerrak Together with IV Risk of reduced reproductive Microgeographical
capacity differences between
fjords (possible)
Kattegat – Uncertain
Vb2, VI, XII2,3, No assessment
XIV2,3
VIIa Reduced reproductive
capacity
VIIb–k, VIII, IX, X, VIId (with IV)
V – Uncertain, low Two distinct populations
in area V (likely)
Haddock I, II1 – Uncertain, high
IIa2, IV IV, IIIa Full reproductive capacity Two populations in IV
(possible)
IIIa, 22–322 IIIa with IV
Vb2, VIa2 Vb Full reproductive capacity Differentiation between
populations in VIa and
Vb (possible)
VIa Full reproductive capacity
VIb2,3, XII2,3, XIV2,3 VIb only Full reproductive capacity
VII, VIII, IX, X VIIa Uncertain
VIIb–k Unknown, decline
Va – Full reproductive capacity
Whiting IIIa – Uncertain
IV, IIa2 IV and VIId Unknown/low Three distinct populations
in IV (possible)
Vb2, VI, XII3, XIV3 VIa Unknown/low
VIb No assessment
VIIa – Uncertain/low
VIIb–k VIIe–k Uncertain
VIIbc Not assessed
VIId with IV Unknown/low
VIII No assessment
IX, X No assessment
European hake IIa2, IV2 IIIa, IV, VI, VII, Full reproductive capacity Differentiation between
VIIIabde VII and IIa (possible)
IIIa, 22–322 IIIa with IV
Vb2, VI, VII, VI, VII with IV
XII3, XIV3
VIIIabde VIIIabd with IV
VIIIc, IX, X VIIIc, IXa Reduced reproductive
capacity

Table 2 Continued.

Plaice IIa2, IV – Risk of reduced reproductive

capacity
22–322 – Unknown
Skagerrak IIIa Unknown, increase
Kattegat IIIa Unknown, increase
Vb2, VI, XII3, XIV3 Vb Not assessed
VI, XII, XIV Not assessed
VIIa – Full reproductive capacity
VIIbc – Unknown/decline
VIIde VIId Uncertain
VIIe Uncertain, decline
VIIfg – Reduced reproductive capacity
VIIhjk – Uncertain
VIII, IX, X
Sole II2, IV2 IV only Reduced reproductive capacity
IIIa, 22–322 IIIa only Full reproductive capacity
Vb2, VI, XII2, XIV3 No assessment
VIIa – Reduced reproductive capacity
VIIbc – Unknown
VIId – Full reproductive capacity
VIIe – Reduced reproductive capacity
VIIfg – Full reproductive capacity
VIIhjk – Unknown
VIIIab VIIIabd Risk of reduced reproductive capacity
VIIIcde, IX, X, VIIId with VIIIab
Greenland I, II1 – Uncertain, low
halibut IIa2, IV2, VI2,3 VI with V, IIa with I
V, XIV4 V, XIV, VI, XII Uncertain, low Differentiation between
Faroe (V) and East
Greenland (XIV)
populations (possible)
Herring I2,3, II2,3 – Full reproductive capacity Two distinct populations
in II (ss) (possible)
22–24 IIIa, 22–24(ss) Uncertain
25–27,28.2,29,32 – Uncertain, increase
28.1 – Full reproductive capacity
30–31 30 Full reproductive capacity
What is this stock? 31 Uncertain
IIIa (ss) with 22–24 Uncertain
IV2,3 IV, VIId, IIIa (as) Risk of reduced reproductive capacity
IVc, VIId – Reduced reproductive capacity
Vb2,3, VIa North2,3, – Reduced reproductive capacity
VIb2,3
VIa South, VIIbc – Reduced reproductive capacity
VIa Clyde – Uncertain
VIIa – Uncertain
VIIe,f – Unknown
VIIghjk – Reduced reproductive capacity
Va – Unknown
Blue whiting I–VIIIabde2,3, Only one stock Full reproductive capacity, risk Two distinct populations;
XII2,3, XIV2,3 of overexploitation VIIg–k and southward/
VIIa–c and northward
(possible)

Table 2 Continued.

VIIIc, IX, X
IV1
Horse IIa2, IV2 IVbc, VIId, IIIa (east) Unknown
Mackerel Vb2, VI, VII, IIa, IVa, Vb, VIa, Unknown, increase
VIIIabde, XII3, XIV3 VIIa–c,e–k, VIIIa–e
VIIIc, IX IXa Unknown
VIIIc with IVa
X no assessment
Mackerel IIa2, IIIa, 22–322, IV Only one stock Reduced reproductive
capacity
IIa3, Vb2, VI, VII,
VIIIabde, XII3, XIV3
IIa1
VIIIc, IX, X,
Vb (Faroese waters)
NEAC, north-east Arctic cod; TAC, total allowable catch; NCC, Norwegian coastal cod. The management areas comprise those spatial
units for which a TAC per stock is set annually (ICES 2007), whereas the assessment area represent the spatial units for which the
scientific stock assessment is carried out. Spring spawners (ss), autumn spawner (as); 1Norwegian waters, 2EU waters, 3international
waters, 4Greenland waters.
decreased dramatically in some management allozymes (Mork et al. 1985) and mitochondrial
areas. For example, the landings of cod in the DNA (Smith et al. 1989). Considerable subpopula-
North Sea (area IV) in 2005 were 12% of those in tion structures were also found on continental shelf
1975 and in the Skagerrak/Kattegat (area III) scale in the NW Atlantic differentiating offshore
only 4%. Therefore, cod stocks are considered to from inshore cod populations and among single
be overexploited in most management areas, and bays (Bentzen et al. 1996; Ruzzante et al. 1996,
plans for restoring the spawning stock sizes are 1998, 2000b; Lage et al. 2004). However, these
under development or have been already imple- findings are based exclusively on microsatellite
mented, such as short-term area closures in the markers (but see also Beacham et al. 2002), and
areas IVc and VIa (Holmes and Wright 2005) and were not supported by mitochondrial DNA markers
days at sea regulations. (Pepin and Carr 1993; Carr et al. 1995).
As shown in Fig. 2 and Table 1, considerable For the NE Atlantic, genetic studies have
effort has been made as the pioneering work of Sick revealed significant differentiation of major cod
(1965a,b) to clarify the possible subdivisions of the populations: NE Arctic, Norwegian coastal, North
Atlantic cod populations on several spatial scales Sea and Baltic cod stocks (Dahle 1991; Nielsen et
using genetic methods. On a North Atlantic-wide al. 2001; Pogson and Fevolden 2003; Sarvas and
scale a clear separation between the NE and NW Fevolden 2005a). Similar to the NW Atlantic,
Atlantic populations, as well as between the genetic differentiation was also found at much
Barents Sea and other populations in the NE smaller spatial scales, indicating a mismatch
Atlantic was found based on mini- and microsate- between population structure and current man-
llite markers (Galvin et al. 1995; Bentzen et al. agement units in some areas.
1996; Hutchinson et al. 2001; O’Leary et al. 2007; The cod in Icelandic waters was proposed to
Skarstein et al. 2007), and on nuclear DNA comprise to a homogeneous population (Árnason et
restriction fragment length polymorphism (RFLP) al. 1992, 2000) and is therefore currently managed
(Pogson et al. 1995; Jónsdóttir et al. 2003). In as one stock (area Va). Recent studies based on the
contrast, a lack of population differentiation bet- non-neutral Pan I locus and microsatellites, how-
ween the NE and NW Atlantic was found with ever, revealed a subdivision into at least two distinct

Figure 1 Management units (ICES divisions and subdivisions) in the NE Atlantic.

Deep-sea fish
Blue ling
Ling Mismatch
Roundnose grenadier No mismatch
Tusk
Sprat
Anchovy
Mackerel
Pelagic fish
Blue whiting
Horse mackerel
Capelin
Bluefin tuna
Swordfish
Herring
Witch flounder
Norway pout
Lemon sole
Dab
Saithe
Brill
Megrim
Pollack
Sandeel
Whiting
Demersal fish
Anglerfish
Skates and rays
Figure 2 Number of genetic popu- Plaice
lation studies per managed species Flounder
(approximately 1980–2008) in the Greenland halibut
Sole
NE Atlantic with mismatch between
Haddock
genetic structure and management Redfish
units indicated. The ‘no mismatch’ Turbot
category also comprise studies where European hake
a detection of mismatches was not Cod
possible, e.g. due to inappropriate 0 10 20 30 40 50 60
spatial scales. Number of references
population in Icelandic waters (Jónsdóttir et al. around the Lofoten (Bergstad et al. 1987), where
1999, 2001, 2002; Imsland et al. 2004; Pampoulie the NEAC intermingle with the NCC population.
et al. 2006). The main fishery areas in autumn are Although assessed separately, the NCC is managed
the feeding grounds NW and east of Iceland. Thus, as part of the Norwegian NEAC fishery. A large part
fisheries are targeting mixed populations originating of the Norwegian cod fishery is targeting the
from the main spawning areas south and NW of spawning components of the NEAC during spring
Iceland (Jónsdóttir et al. 2007). (Nakken et al. 1996), which results in catches of
The most important cod stocks in the NE Atlantic mixed stocks (Wennevik et al. 2008). The manage-
are found along the Norwegian coast and the ment takes this into account by adding an expected
Barents Sea (areas I and II) where two stocks are yield of 20 000 tons of NCC to the TAC of the
assessed separately; the migratory NE Arctic cod NEAC. Additionally, several fjord areas were closed
(NEAC) and the more stationary Norwegian coastal for direct cod fishing to reduce the exploitation on
cod (NCC). Such subdivision was supported by NCC and to displace fishing to cod outside the fjords
genetic studies using haemoglobin (Dahle and where the proportion of NEAC is higher (ICES,
Jørstad 1993; Husebø et al. 2004), mtDNA (Dahle 2007). For the NCC, recent studies suggest a further
1991), microsatellites (Skarstein et al. 2007; Westg- subdivision on a microgeographical scale and, thus
aard and Fevolden 2007), and especially the non- a mismatch between management units and popu-
neutral Pan I locus (Fevolden and Pogson 1997; lation structure, showing significant population
Berg et al. 2005; Sarvas and Fevolden 2005a). The differentiation among fjords (Sarvas and Fevolden
NEAC migrates from their offshore feeding areas in 2005b; Dahle et al. 2006; Skarstein et al. 2007),
the Barents Sea to the more coastal spawning areas which was also found for populations among fjords

of the Skagerrak (Knutsen et al. 2003; Jorde et al. indicating population differentiation between banks
2007). Although the finding of this microscale (Nantucket Shoals, Grand Banks), whereas only a
differentiation is based on a variety of genetic weak cline along the coast from north to south was
markers and adequate sampling strategies, the detected by using mitochondrial DNA (Zwanenburg
temporal stability of the population structure was et al. 1992).
hardly addressed, and is still under debate (Table 1). Haddock in the NE Atlantic is currently managed
Furthermore, for the North Sea stock (area IV), based on a separation between seven management
which is managed together with the EU waters of units (Table 2). Although genetic data underpin the
area IIa as one unit [but assessed together with division between stocks of area VIb (Rockall) and
the Skagerrak (IIIa) and the English Channel VIa (west of Scotland), a mismatch may occur in
(VIId), Table 2], Hutchinson et al. (2001) found other areas such as the North Sea (area IV)
at least three to four distinct cod populations: (Table 2). Current assessment procedures already
Bergen, Moray Firth, Flamborough Head and distinguish between populations of the management
Southern Bight (see also Skarstein et al. 2007), areas VIa and Vb, but an aggregated TAC is still
but here, too, the temporal stability of the differen- used in these areas (ICES, 2005a).
tiation remains uncertain. Nevertheless, such small-
scale subdivision of cod populations is confirmed by Other demersal roundfish species
tag recapture studies, which found evidence for Other demersal species managed via TACs in the NE
limited migration between nursery and spawning Atlantic are saithe (Pollachius virens, Gadidae),
areas as well as resident adult populations in pollack (Pollachius pollachius, Gadidae), whiting
Scottish coastal waters (Neat et al. 2006; Wright (M. merlangus, Gadidae), Norway pout (Trisopterus
et al. 2006a,b). esmarkii, Gadidae) and European hake (M. merluc
Thus, despite the equivocal conclusions depend- cius, Merluccidae). With the exception of European
ing on markers, temporal replication and the hake, these species are distributed throughout the
sampling strategy employed (Table 1), a mismatch boreal and temperate regions of the NE Atlantic. Of
between population structure of cod and manage- these species, saithe is commercially the most
ment and assessment units seems to be likely in important one, with more than 440 000 tons
several regions of the NE Atlantic (Table 2). landed in the NE Atlantic in 2005. The other four
species are of secondary commercial importance;
Haddock together they account for <100 000 tons landed in
Haddock (M. aeglefinus, Gadidae) is widespread 2005. However, the landings of whiting and Nor-
throughout the deeper waters of the temperate way pout have decreased dramatically in recent
North Atlantic. It is exploited in mixed trawl and decades. Landings of whiting decreased from more
seine fisheries, with more than 282 000 tons than 200 000 tons in the early 1970s to 33 000
caught in the NE Atlantic in 2005, mainly by tons in 2005, and landings of Norway pout
Scottish, Norwegian and Icelandic fishing fleets. decreased from 800 000 tons in 1974 to
Despite the commercial importance of haddock, 22 500 tons in 2004. Consequently, the fishery
only limited information is available on genetic on Norway pout was closed in the management
population structure within the Atlantic (Table 1). area IV (North Sea), which in 2005 is the main
For the NE Atlantic, only two studies investigated fishing area for this species (ICES, 2005a).
genetic population structure leading to incongruent No genetic information was found for saithe and
results. Jamieson and Birley (1989) detected signif- Norway pout, and only one study investigated the
icant differentiation between the north-eastern population structure of pollack within the NE
North Sea/Faroe and the north-western North Sea, Atlantic, with no significant differentiation being
as well as between these populations and the detected (Charrier et al. 2006b).
Rockall population based on allozyme data. In Whiting is caught as part of a mixed fishery
contrast, Giæver and Forthun (1999) could not operating in the North Sea throughout the entire
find significant differentiation among haddock pop- year, and is currently managed and assessed as a
ulations of Norwegian coastal waters and fjords, single unit (Table 2). However, significant genetic
Iceland, Barents Sea and the North Sea using structuring was recently found in the North Sea,
allozymes. Microsatellite markers have so far only which is relatively similar to that found for cod
been used in the NW Atlantic (Lage et al. 2001), (Hutchinson et al. 2001), with three distinct whiting

populations in the areas of the Southern Bight, the procedures distinguish among stocks of the North
Flamborough Head and the Dogger Bank/Norwe- Sea (area IV), English Channel (area VIId) and the
gian coast (Charrier et al. 2007). The temporal Skagerrak/Kattegat (area IIIa). Tagging experi-
stability of the genetic population differentiation is ments showed that plaice spawning in the Channel
not yet assessed, but previous studies of parasitic mix with North Sea spawners during the feeding
infestation and tagging data also suggested popula- season in the North Sea (Houghton and Harding
tion differentiation within the North Sea (e.g. Hislop 1976). Although fisheries for plaice are primarily
and MacKenzie 1976; Pilcher et al. 1989). Further- targeting spawning components in late winter early
more, there is some evidence for complex small-scale spring, it is also carried out on the feeding grounds
population structure in whiting within the Irish Sea (Poos and Rijnsdorp 2007) and, thus might target
(area VIIa) from sources such as otolith microchem- mixed populations (Kell et al. 2004). However,
istry (e.g. Geffen et al. 2003), though such microge- genetic studies using microsatellite markers
ographic differentiation is not yet considered in revealed no significant differentiation among conti-
current management and assessment measures. nental shelf locations ranging from the Bay of
Several studies have explored genetic population Biscay to Norway. Only the Icelandic population
structure in European hake (Table 1), which is were significantly different from the continental
widely distributed in the Mediterranean and along shelf locations, with the deep water between Iceland
the Atlantic coast from Morocco to Norway. A clear and the shelf functioning as a barrier to dispersal
differentiation between hake populations of the (Hoarau et al. 2002, 2004). However, mtDNA data
Mediterranean and the Atlantic was found by all indicated that populations in the North Sea and
studies whether based on allozyme, mtDNA or Irish Sea were weakly distinguishable from Norway,
microsatellite markers (Table 1). Present assess- the Baltic and the Bay of Biscay (Hoarau et al.
ment of hake in the Atlantic is based on distinct 2004). Recent tagging studies indicated three dis-
‘northern’ (mainly area IV, VI and VII) and ‘south- crete feeding aggregations of plaice in the North Sea
ern’ (area VIIIc and IX) stocks, but such a division is during the non-breeding season, with subsequent
not supported by current genetic data (Lundy et al. mixing in the spawning grounds (Hunter et al.
1999, 2000; Castillo et al. 2005). Furthermore, 2004), which is opposite to the expected pattern.
Lundy et al. (1999) found significant differentiation Nonetheless, such feeding aggregations do not
between Norwegian coast and Celtic Sea samples, appear to be genetically different (Hoarau et al.
which are currently managed as a single stock. 2002, 2004).
Although the temporal stability of this structure On a regional scale, Watts et al. (2004) investi-
remains unclear, these results indicate a more gated genetic population structure of juvenile plaice
complex population structure in the Atlantic than in the Irish Sea, where the plaice population is
previously suggested. managed as a single stock (area VIIa). Results also
revealed no differentiation within the area based on
Plaice microsatellite markers. On the other hand, the
The European plaice (Pleuronectes platessa, Pleuro- possibility of inbreeding both in the North Sea and
nectidae) is economically an important target spe- in Iceland (Hoarau et al. 2005), together with the
cies for the demersal fisheries in the NE Atlantic and detection of related juveniles on nursery grounds,
can be found from the western Mediterranean to the suggest that there might be small-scale family
White Sea and Iceland. Plaice is mainly exploited in structuring on the spawning ground.
a mixed flatfish fishery together with sole by beam
and otter trawling, with almost 70% of the Sole
76 000 tons plaice landed in 2005 caught in the The common sole (Solea solea, Soleidae) is a south-
North Sea (area IV). ern flatfish species that reaches its northern distri-
Mature plaice in the North Sea migrates between bution limits in the central North Sea. It is of high
distinct spawning grounds in winter and feeding commercial value with landings over 29 000 tons
grounds in summer (de Veen 1978; van Beek et al. in NE Atlantic in 2005. The most important fishing
1989). The repeat homing behaviour to the spawn- fleets targeting sole mainly by mixed beam and otter
ing grounds with a fidelity of up to 100% (Hunter trawl fisheries are those from the Netherlands and
et al. 2003) has led to the prediction of distinct France accounting for more than 65% of the
subpopulations in this area. Current management landings in 2005.

Similar to plaice, sole in the North Sea (area IV), Only Knutsen et al. (2007) found a weak differen-
is currently managed as one unit where more than tiation among Greenland halibut populations with-
50% of the yearly landings is caught. Despite in the NE Atlantic by using microsatellites,
indications for different sub-population of sole in suggesting a differentiation between the Faroe (area
the North Sea based on tagging experiments and V) and East Greenland stocks (area XIV), which are
egg distribution (Rijnsdorp et al. 1992), no popu- currently managed as one unit (Table 2).
lation differentiation was found with genetic meth- Genetic differentiation in turbot has been found
ods (Table 1). The Atlantic sole population appears between populations of the Baltic and the Atlantic/
to be a single panmictic unit ranging from Denmark North Sea connected by a hybrid zone (Nielsen et al.
to Portugal based on allozymes (Kotoulas et al. 2004), whereas within these regions, limited or no
1995a) and polymorphic exon-primed intron-cross- genetic differentiation was found (Blanquer et al.
ing markers (Rolland et al. 2007). Only Exadactylos 1992; Bouza et al. 1997, 2002; Coughlan et al.
et al. (1998, 2003) detected genetic differentiation 1998; Nielsen et al. 2004; Florin and Höglund
among continental European populations (German 2007). A similar separation between the Baltic and
Bight and Bay of Biscay) and the British Isles the North Sea was found for the European flounder
populations using DNA RAPD and allozymes, with (Hemmer-Hansen et al. 2007; Larsen et al. 2007).
an apparent barrier to gene flow in the English However, both species, turbot and European floun-
Channel. However, the latter studies are based on der, are up to now managed by a TAC for the area
low marker quality and no temporal replication was IV/EU waters of IIa only and no stock assessment is
carried out (Table 1). Furthermore, only two sites carried out.
within the management area IV were included,
necessitating higher sampling intensity and spatial Redfish
coverage before definitive information on popula- Three species of redfish are commercially exploited
tion structure can be provided. in the NE Atlantic, the golden redfish (Sebastes
marinus, Scorpaenidae), the beaked redfish (Sebastes
Other flatfish species mentella, Scorpaenidae) and the Acadian redfish
Several other flatfish species are managed via TACs (Sebastes fasciatus, Scorpaenidae). In total,
in the NE Atlantic, but most are of minor commer- 134 400 tons mainly of golden and beaked redfish
cial importance, with landings £15 000 tons in were landed in the NE Atlantic in 2005. The
2005 such as common dab (Limanda limanda, Acadian redfish has been only of minor commercial
Pleuronectidae; 15 300 tons), lemon sole (Micro- value mainly in Icelandic waters. Officially reported
stomus kitt, Pleuronectidae; 12 200 tons), witch landing statistics for the NE Atlantic do not divide
flounder (Glyptocephalus cynoglossus, Pleuronecti- the redfish catches by species. Thus, for the assess-
dae; 9500 tons), megrim (Lepidorhombus whiffiago- ment of redfish stocks, various information sources
nis, Scophthalmidae; 3600 tons), turbot (Psetta about catch locations are used to split landings data
maxima, Scophthalmidae; 5200 tons) and brill into species (ICES, 2005a), whereas the manage-
(Scophthalmus rhombus, Scophthalmidae; 2600 ment is only based on a lumped TAC for the genus
tons). Only the landings of European flounder Sebastes.
(Platichthys flesus, Pleuronectidae; 24 100 tons) Due to the difficulties with morphologically based
and Greenland halibut (Reinhardtius hippoglossoides, determination of redfish species, genetic methods
Pleuronectidae; 42 200 tons) exceeded 20 000 have been in the past mainly used for species
tons in 2005. discrimination (Nedreaas and Nævdal 1989, 1991;
Studies on genetic structure are rare for most Sundt and Johansen 1998; Roques et al. 1999;
species, and an indication for a mismatch between Johansen and Dahle 2004). Nevertheless, some
management units and genetic population structure studies have also shown genetic differentiation
in the NE Atlantic was found only for Greenland within species mainly on large spatial scales. Roques
halibut (Table 1). No studies have been found for et al. (2002) detected three distinct populations of
lemon sole, dab and witch flounder. A lack of S. mentella across the whole North Atlantic by using
significant differentiation within the NE Atlantic has microsatellite markers: an Eastern (Norway and
been reported for brill (Blanquer et al. 1992), Barents Sea), a Western (Gulf of St. Lawrence and
megrim (Garcia-Vazquez et al. 2006) and Greenland Newfoundland) and a pan-oceanic population rang-
halibut (Vis et al. 1997; Igland and Nævdal 2001). ing from Labrador to the Faroe Islands (see also

Johansen et al. 2000a). Such separation supports thornback rays by using microsatellites and mtDNA
current management and assessment practices in (Chevolot et al. 2006b), whereas genetic structure
the NE Atlantic that distinguish between the NE in the southern North Sea, English Channel and
Arctic (areas I and II) and the Faroe Islands, Iceland Irish Sea was less clear. Weak but significant
and east Greenland (areas V, VI, XII and XIV). differentiation was found, but it was temporally
Furthermore, for stock assessment of S. mentella a and spatially unstable, and the absence of differen-
‘demersal’ population on the shelf of Greenland, tiation among some distant populations suggests
Faroe and Iceland is treated separately from a that a part of the thornback ray population may
‘pelagic’ population in the Irminger Sea and adja- migrate over wide areas (Chevolot et al. 2006a).
cent waters. Such separation is marked by the Such views were supported by tagging studies,
‘redfish line’ along the 500 m isobath in Icelandic showing on the one hand, a seasonal homing
waters. In contrast, genetic population structure migration of thornback rays to specific spawning
based on allozyme markers showed separation grounds, but on the other hand, a migration to
between an ‘oceanic’ and a ‘pelagic deep-sea’ type feeding grounds over wide areas of the southern
within the ‘pelagic’ population, but not between the North Sea (Walker 1997; Hunter et al. 2005,
‘pelagic deep-sea’ and the ‘shelf deep-sea’ (demersal) 2006). A lack of population differentiation has
population (Johansen et al. 2000a). The different been reported for the thorny skate in the North
hypotheses of population structuring of S. mentella Atlantic ranging from Newfoundland to Iceland and
in this region and the consequences for manage- Norway. Only the Kattegat population was
ment units have been discussed (Saborido-Rey et al. genetically different from other populations
2004; ICES, 2005b). Evidence for hybridization (Chevolot et al. 2007).
between S. mentella and S. fasciatus found in the NW
Atlantic (Desrosiers et al. 1999; Roques et al. 2001)
Pelagic fish species
renders population identification even more com-
plicated. However, in the first instance, methods for Herring
the identification of Sebastes species are needed to The Atlantic herring (C. harengus, Clupeidea) is one
enable a species based management of redfish, such of the most important pelagic species in the North
as for example the application of DNA barcoding Atlantic, with more than 2 million t landed in the
(Costa and Carvalho 2007). NE Atlantic in 2005. It is exploited by using various
types of fishing gear such as purse seine, mid-water
Rays and skates trawl, pair and otter trawl mainly by the Norwegian
Rays and skates are of secondary commercial and Icelandic fleet (about 50% of annual landings).
importance in the NE Atlantic and only small Atlantic herring aggregates to spawn at discrete
tangle net and long-line fisheries are specifically sites, most are presumed to return to the same
targeting rays off the British coast. However, most spawning ground every year, thereby representing
rays and skates are taken as bycatch in nets, long- repeat spatial spawners (Parrish and Saville 1965).
lines, beam trawl and otter trawl (Walker and The timing of spawning differs with spawning
Heessen 1996; Hunter et al. 2006), resulting in component, and different spawning components
almost 26 000 tons landed in 2005. Due to their have different morphometric features (McPherson
slow growth rate, low fecundity and late matura- et al. 2001). Such differences are often used to
tion, rays and skates are highly vulnerable to describe ‘races’ of herring (Zijlstra 1969), though
fisheries exploitation. Since 1997 they are managed they appear mainly to represent variation in meris-
by an aggregated TAC for EU waters in area IV and tic characteristics of each cohort resulting from
II only, but more than 75% of the landings were temperature at spawning and larval development
caught in the southern and western areas VII, VIII (Taning 1951; Hempel and Blaxter 1961). There is
and XI. extensive mixing between spawning components
Data on genetic population structure can be and stocks during the feeding aggregations, during
found for two species only: the thornback ray (Raja the juvenile stages and sometimes during over
clavata, Rajidae) and the thorny skate (Amblyraja wintering (Blaxter and Hunter 1982; Brophy and
radiata, Rajidae). Large-scale differentiation among Danilowicz 2002).
the Mediterranean, the Azores and the European Thus, herring is characterized by a high level of
continental shelf was found for populations of temporal and spatial stock complexity (McQuinn

1997). Although considerable effort has been made (de Barros and Holst 1995). However, the finding
to investigate genetic stock structure of herring in of significant genetic differentiation by Shaw et al.
the Atlantic (Table 1), temporal and spatial struc- (1999) is based on a rather small number of
ture is still under debate. Even genetic differentia- microsatellite loci and no temporal replication was
tion on a large scale between NW and NE Atlantic is carried out (Table 1). The genetically distinct her-
equivocal (McPherson et al. 2004; Bekkevold et al. ring population found in the Basfjord based on
2005; Mariani et al. 2005). The extensive migration allozymes and mitochondrial DNA by Jørstad et al.
and the consecutive mixing of adult herring (1991, 1994) was not confirmed by other studies
together with the possible existence of genetically using microsatellites (Turan et al. 1998; Shaw et al.
distinct spawning waves in some areas (McPherson 1999).
et al. 2003; Jørgensen et al. 2005b) render their
management difficult. Capelin
Within the North Sea several herring subpopula- The capelin (Mallotus villosus, Osmeridae) is a small
tions were distinguished based on meristic param- pelagic and short-lived species distributed over the
eters, spawning sites and season (Cushing 1967; boreal waters of the North Atlantic and North
Iles and Sinclair 1982). Such subdivision was, Pacific oceans. It is of major importance as a prey
however, not supported by recent genetic studies species for many other fish species (e.g. cod and
based on microsatellites that indicate genetically salmon), seabirds and marine mammals and,
indistinguishable spawning aggregations of herring as such, is a keystone species in the food web of
in the North Sea (Mariani et al. 2005; Ruzzante et the boreal marine ecosystems (Friis-Rødel and
al. 2006), thereby reinforcing the current manage- Kanneworff 2002; Rose 2005a and references
ment of North Sea herring as a single management therein). The fishery targeting capelin in the NE
unit. Nevertheless, Mariani et al. (2005) found Atlantic is mainly for reduction purposes, with more
slight genetic differences between the herring pop- than 85% of the 692 000 tons capelin landed in
ulation in the English Channel (Downs herring) and 2005 caught by the Icelandic fleet.
the remaining North Sea population, which was The management of capelin in the NE Atlantic is
already taken into account by a sub-TAC for based on two stocks, the Barents Sea (areas I and II)
subarea IVc and VIId within the North Sea TAC. and the Greenland/Iceland stock (areas V and XIV).
Despite extensive mixing of larval and adult life Although capelin spawns in spatially and tempo-
stages of herring on nursery and feeding grounds in rally separated aggregations throughout its distri-
the Skagerrak, significant genetic differentiation bution range, genetic studies were almost solely
was found between North Sea and Baltic spawning focused on large-scale differentiation between pop-
populations (Bekkevold et al. 2005; Ruzzante et al. ulations (Table 1). Genetic differentiation between
2006) and between populations within the Baltic NW and NE Atlantic populations was found based
Sea (Jørgensen et al. 2005a) based on microsatel- on microsatellites and mitochondrial DNA (Dodson
lites, indicating a strong structuring effect of envi- et al. 1991; Birt et al. 1995; Røed et al. 2003),
ronmental gradients (such as salinity) on herring whereas neither a separation between different
populations (Bekkevold et al. 2005). However, the spawning aggregations (beach and bottom spaw-
different assemblages identified by Jørgensen et al. ners) in the NW Atlantic based on mitochondrial
(2005a) correspond roughly with the main man- DNA (Dodson et al. 1991) nor a separation between
agement units in the Baltic Sea. Barents Sea and Norwegian fjord populations by
The Norwegian spring spawning herring in the using allozymes (Mork and Friis-Sørensen 1983)
Barents Sea and Norwegian Sea (areas I and II) is could be determined.
commercially the most important stock, with almost
1 million ton landed in 2005, and is currently Blue whiting
managed as a single unit. Thus, the differentiation Blue whiting (M. poutassou, Gadidae) is a pelagic
between a northern and a southern population gadoid species of high commercial importance since
within the Norwegian spring spawners found by stocks of this species have been at historically high
Shaw et al. (1999) indicate a mismatch between levels in recent years, with more than 2 million tons
population structure and management unit. Such landed in the NE Atlantic in 2005. The fishery on
differentiation coincides with morphological differ- blue whiting is mainly targeting spawning and
ences between northern and southern herring post–post-spawning aggregations along the shelf

edge and banks west of the British Isles. Despite its mainly based on morphometrics, parasites and life
commercial relevance, only limited information history traits (Abaunza et al. 2008).
exists about the genetic population structure of Another clupeid species of commercial interest,
blue whiting (Fig. 2; Table 1). Most genetic data mainly for reduction purposes, is the sprat
support differentiation only at the extremes of the (S. sprattus). The total abundance of sprat has
distribution range, that is, between Barents Sea and increased dramatically in the Baltic Sea in the last
Mediterranean (Mork and Giæver 1995; Giæver decade, where about 45% of the 733 000 tons
and Stien 1998; Ryan et al. 2005). This is in landed sprat was caught in 2005. Stock manage-
accordance with the current management of blue ment is based on four units separating the North Sea
whiting as a single stock in the NE Atlantic. (IV), the Skagerrak (IIIa), the English Channel (VIId)
However, modelling of larval drift suggest the and the Baltic Sea (22–32). Despite the commercial
existence of at least a northern and a southern importance of sprat especially in the Baltic Sea, no
population (Bartsch and Coombs 1997; Skogen et published study of the genetic population structure
al. 1999), which was recently supported by genetic is available up to now (Table 1).
studies using microsatellites (Was et al. 2008),
indicating a mismatch between population struc-
Spatial mismatch – implications for fisheries
ture and management units (Table 2).
management
Other pelagic species Despite the substantial increase in using genetic
Other pelagic species managed via TACs in the NE markers for exploring population structure in recent
Atlantic are the mackerel (Scomber scombrus, Scom- decades, our overview indicates that published
bridae), the horse mackerel (Trachurus trachurus, genetic data are relatively meagre or even lacking
Carangidae), the sprat (Sprattus sprattus, Clupeidea), for many commercially exploited and quota-man-
the European anchovy (Engraulis encrasicolus, aged fish species in the NE Atlantic (Fig. 2, Table 1).
Engraulidae) as well as two species with a global Only for a few exemplary species such as cod and
distribution range, the swordfish (Xiphias gladius, herring, are sufficient genetic data available to
Xiphiidae) and the bluefin tuna (Thunnus thynnus, provide information on relevant spatial scales for
Scombridae) (Table 1). integration into management strategies. Such a lack
The mackerel (S. scombrus) and the horse of knowledge cannot be compensated by the
mackerel (T. trachurus) are pelagic shoaling species extrapolation of population structure from well-
of commercial interest. The annual landings of known species to others, even if the species are
mackerel were 447 000 tons and of horse mackerel closely related (Ward 2000). The apparent weak
204 000 tons in the NE Atlantic in 2005. Both genetic differentiation found for ray species, with a
species are managed based on three stock units in low fecundity and oviparous or ovoviviparous
the NE Atlantic. For the mackerel the Western stock reproduction, and for most other marine fish species
(areas VI, VII and VIIIa,b,d,e) was found to be with a high fecundity and high distribution capacity
genetically different from the Southern stock (areas due to pelagic larvae, demonstrates that life history
VIIIc and IXa) and the North Sea stock (areas IV traits are also an inappropriate indicator of genetic
and IIIa) based on mitochondrial DNA (Nesbø et al. population structure. However, the detection of
2000). As the spawning areas of mackerel are temporally stable genetic differentiation clearly
widely spread, and with the exception of the North indicates reproductively distinct assemblages.
Sea, not entirely distinguishable, current stock Such apparently reproductively distinct units
assessment procedures consider the different spawn- should be regarded as the minimum resolution of
ing components as one single stock for practical populations that need to be managed and con-
reasons (ICES, 2007). served. Nevertheless, the estimation of patterns in
For the horse mackerel (T. trachurus) no genetic temporal genetic stability remains relatively rare
differentiation was found among the three stocks compared to spatial studies (Table 1), though it
using allozymes, mitochondrial DNA and microsat- remains a primary way of assessing the biological
ellites (Borges et al. 1993; Karaiskou et al. 2004; significance of management units.
Cimmaruta et al. 2008; Comesana et al. 2008; Despite mostly insufficient data, the mismatch
Kasapidis and Magoulas 2008) and, thus the between genetic population structure and the cur-
distinction for management and assessment is rent management units found for six species

strongly emphasize the need for a re-evaluation of morphometrics and microchemistry and other mor-
these units and the appropriateness of current phometric characteristics, genetic methods used for
management techniques. Under the precautionary mixed stock analysis (MSA) or individual assign-
approach, any partly conflicting conclusions con- ment tests were in the past mainly applied to
cerning the genetic population structure of a multiple stocks of anadromous fish species (Utter
species, as shown above, must not prevent man- and Ryman 1993; Carvalho and Hauser 1994;
agement being developed in relation to the potential Ruzzante et al. 2000a; Beacham et al. 2006). For
underlying structure of populations. As stated in the marine species the relative proportion of different
United Nations Straddling Stocks Agreement about cod populations mixing in overwintering areas in
the precautionary approach (UN, 1995) ‘States the NW Atlantic was estimated by Ruzzante et al.
shall be more cautious when information is uncer- (2000a). Here not only the proportion of the various
tain, unreliable or inadequate. The absence of cod populations could be estimated but also the
adequate scientific information shall not be used temporal stability of this structuring was demon-
as a reason for postponing or failing to take strated over a 2-year period (see also Ruzzante et al.
conservation and management measures’. A 2006; Bekkevold et al. 2007; Wennevik et al.
short-term pragmatic solution to buffer against the 2008). Therefore, it seems possible that fisheries
uncertainty regarding the consequences of ignoring management could be designed around the spatial
complex population structures would be to reduce and temporal population structure within the sep-
fishing mortality in those management areas where arated spawning grounds and the areas where
a mismatch between management units and popu- populations are mixed (Ruzzante et al. 2000a; ICES,
lation structure is evident. 2005c). In this respect appropriate stock assessment
A major challenge in implementing genetic data models will be of particular importance, since
into management considerations is the mixing of current models are mainly based on single-species
distinct populations of migratory fish species at stock assessment even in areas where mixed stocks
specific fishing grounds. Many fisheries in the NE are targeted. Hitherto, only few modelling
Atlantic do not exploit a single population, but a approaches exist that account for multiple stocks
mixture of different populations depending on the and the non-uniform exploitation of stocks. The
time of the year and the fishing area. For example, most comprehensive one is probably the seasonally
larval and adult life stages of North Sea and Baltic structured population dynamics model developed by
spawning populations of Atlantic herring are mix- Cunningham et al. (2007), which considers the
ing in nursery and feeding grounds in the Skagerrak multi-stock, multi-fleet and multi-area characteris-
(e.g. Clausen et al. 2007), making discrimination tics of the exploitation of mixed stocks. A further
between populations within the catches rather prerequisite for the integration of MSA or individual
difficult. As an operational response to difficulties assignment tests into management procedures is the
in assigning mixed catches to specific herring existence of adequate genetic data of the distinct
populations in Canadian waters, a within-season baseline populations, which is not the case for many
management approach was adopted for herring of the species managed in the NE Atlantic (Fig. 1).
stocks, where fishing quotas are set after herring Furthermore, the utility and power of assignment
populations were surveyed and assessed within each tests depend on the degree of genetic differentiation
season (Stephenson 1999; Smedbol and Stephenson among populations, number of loci and their degree
2001). of polymorphism as well as sample size (Hansen et
Thus, even if the spatial genetic population al. 2001; Hauser et al. 2006). Cornuet et al. (1999)
structure of the spawning components is known showed that a 100% correct assignment rate was
and integrated into fisheries management, a mis- achieved by using a Bayesian method with 10
match between management units and the popula- microsatellite loci on 30–50 individuals of 10
tions is still possible due to the temporal mixing of populations when the Fst is near 0.1. As genetic
distinct populations. The relative contribution of differentiation for many species mentioned above is
each population within a specific area should be small and often do not exceed an Fst of 0.1,
documented and taken into account in manage- sampling schemes and especially the numbers of
ment advice and stock assessment. Besides a variety loci have to be extended (Hansen et al. 2001).
of classical methods used to estimate relative stock The current deficiency of genetic data is perhaps
composition, such as biological markers, otolith of limited significance unless more flexible manage-

ment procedures allow the incorporation of such enable sustainable fisheries, aspects of population
data into management decisions that delimit spatial complexity and genetic diversity remain to be fully
management units. In this regard, Halliday and implemented. The implementation of an EAM will,
Pinhorn (1990) suggest a hierarchical graticule by necessity have to include a variety of social,
system of data collection to improve the flexibility of economic, biological, jurisdictional and political
fisheries management. However, a first step towards factors; ecological constraints will only be one
a more integrative approach might be the improve- component. Nevertheless, within ecosystem-based
ment of integration and accessibility of existing and management approaches, future fisheries activities
future genetic data as proposed by the ‘ICES will be managed as part of a spatial planning
Working Group on the Application of Genetics in framework together with other sectoral activities
Fisheries and Mariculture’ (ICES, 2006). (e.g. Douvere and Ehler 2007; Douvere et al. 2007),
It was often requested that fisheries management thereby reinforcing the need for spatial manage-
should develop towards simpler management pro- ment units aimed at protecting ecosystem properties
cedures that are pragmatic, cost-effective and pre- and components. Within the context of an appar-
cautionary (e.g. Cotter et al. 2004; Kelly and ently inadequate biological basis of management
Codling 2006). The implementation of complex unit delimitation in the NE Atlantic, application of
and dynamic population structures and genetic an ecosystem-based approach could be an opportu-
diversity issues seem to contradict the development nity for greater integration of genetic population
of less complex management approaches. To merge structure and other levels of biological diversity
these two aspects within new management strate- within fisheries management.
gies should be a primary task for fisheries manage-
ment. Approaches that are based on a greater
Acknowledgements
understanding of the underlying complexity of
populations will either require much more genetic We thank Gary Carvalho and the anonymous
information or use management techniques that referees for their valuable input. This research was
whilst simple, reflect an understanding of the supported by NWO-Prioriteit Programma ‘Sustain-
underlying population dynamics and complexity. able Use and Conservation of Marine Living
On a local scale, community-based co-management Resources’, Project Nr. 885-10-317.
might be an approach to address the current
mismatch between the large-scale management
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Reiss Et Al. 2009. Genetic Population Structure Mismatch

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Reiss Et Al. 2009. Genetic Population Structure Mismatch

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F I S H and F I S H E R I E S , 2009, 10, 361–395

Genetic population structure of marine fish: mismatch

Henning Reiss1, Galice Hoarau1, Mark Dickey-Collas2 & Wim J. Wolff1

2009 Blackwell Publishing Ltd DOI: 10.1111/j.1467-2979.2008.00324.x 361

management boundaries (Halliday and Pinhorn

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(1) Norw (2), Baltic (2)

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2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

2009 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 10, 361–395

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Management Mismatch with Mismatch with genetic

Cod I, II1 NEAC Full reproductive capacity, Differentiation between

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Management Mismatch with Mismatch with genetic

Plaice IIa2, IV – Risk of reduced reproductive

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Management Mismatch with Mismatch with genetic

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Figure 1 Management units (ICES divisions and subdivisions) in the NE Atlantic.

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