ICES Journal o f
ICES
International Council for
the Exploration of th e Sea
Conseil International pour
l'Exploration de la Mer
Marine Science
ICES Jo u rn a l o f M arine Science (2014), 71(3), 6 4 8 -6 6 5 . doi: 10.10 9 3 /ic e sjm s/fst 152
Contribution to the Themed Section: 'The Value of Coastal Habitats for Exploited Species'
Review
R ochelle D. Seitz1* H äkan W e n n h a g e 2, Ulf B erg strö m 3, R om uald N. Lipcius1, a n d T om Y se b a e rt4,5
Virginia Institute o f Marine Science, College o f William & Mary, PO Box 1346, Gloucester Point, VA 23062, USA
2D epartment o f Aquatic Resources, Institute o f Marine Research, Swedish University o f Agricultural Sciences, Turistgatan 5, 453 30 Lysekil, Sweden
3D epartment o f Aquatic Resources, Institute o f Coastal Research, Swedish University o f Agricultural Sciences, Skolgatan 6, 742 42 Öregrund, Sweden
AMARES - Institute fo r Marine Resources and Ecosystem Studies, PO Box 77, 4400 AB Yerseke, The Netherlands
5Netherlands Institute fo r Sea Research (NIOZ), PO Box 140, 4400 AC Yerseke, The Netherlands
*Corresponding author: tel: + 1 804 684 7698; fax: + 1 804 684 7399; e-mail: seitz@vims.edu
Seitz, R. D., W ennhage, H., Bergström, U., Lipcius, R. N., and Ysebaert, T. 2014. Ecological value o f coastal habitats for commercially and ecologically
im portant species. - ICES Journal of Marine Science, 71: 648-665.
Received 7 June 2013; acce p te d 20 A ugust 2013; advance access publication 14 O c to b e r 2013.
M any exploited fish a n d m acro in v e rteb ra te s t h a t utilize th e coastal zone have declined, a n d th e c auses o f th ese declines, a p a rt from over­
fishing, rem ain largely unresolved. D egradation o f essential h a b ita ts has resu lted in h a b ita ts th a t are n o longer a d e q u a te to fulfil nursery,
feeding, o r re p ro d u ctiv e functions, y et th e d egree to w hich coastal h a b ita ts are im p o rta n t for exploited species has n o t been quantified.
Thus, w e review ed a n d synthesized literature o n th e ecological value o f coastal h a b ita ts (i.e. seagrass beds, shallow su btidal a n d intertidal
habitats, kelp beds, shallow o p e n w a ter habitats, saltm arshes, m ussel beds, m acroalgal beds, rocky b o tto m , a n d m aricu ltu re beds) as feeding
grounds, nursery areas, spaw ning areas, a n d m igration ro u te s o f 59 taxa, for w hich th e In ternational C ouncil for th e Exploration o f th e Sea
(ICES) gives m a n a g e m e n t advice, a n d a n o th e r 12 com m ercially o r ecologically im p o rta n t species. In addition, w e provide d etailed infor­
m atio n on coastal h a b ita t use for plaice (Pleuronectes platessa), c o d (Gadus m orhua), brow n sh rim p (Crangon crangon), a n d European
lobster (H om arus g a m m a ru s). Collectively, 44% o f all ICES species utilized coastal habitats, a n d th e se stocks c o n trib u te d 77% o f th e c o m ­
m ercial landings o f ICES-advice species, indicating th a t coastal h a b ita ts are critical to p o p u latio n persistence a n d fishery yield o f ICES
species. T hese findings will aid in defining key h a b ita ts for p ro te c tio n a n d re sto ratio n a n d provide baseline in form ation n e e d e d to
define know ledge gaps for quantifying th e h a b ita t value for e xploited fish a n d invertebrates.
Keywords: feeding, fisheries, migration, nursery, reproduction, spawning.
Introduction
Habitat and exploited species
M any exploited species are experiencing p o p u la tio n declines. In
a d d itio n to overfishing, h a b ita t changes m ay po ten tially be involved
to a large extent in these declines (W o rm et ah, 2006). C onsequently,
a m ajo r effort is un d erw ay globally to a d o p t a n ecosystem -based a p ­
p ro ach to fishery m anagem ent, w hich includes the effects o f fishing
o n h a b ita t quality (e.g. H ollow ed et al., 2011), the use o fm a rin e p ro ­
tected areas (M PAs) based o n h a b ita t characteristics (e.g. L ink et a t,
2011) a n d th e effects o f h a b ita t availability o n fishery yield
(M cC lanahan et al., 2011).
C oastal habitats are th rea te n e d b y a n th ro p o g e n ic stressors, in ­
c luding coastal develo p m en t a n d h a b ita t d eg rad atio n (K ennesh,
2002; K em p et al., 2005; Lotze et al., 2006; A iroldi a n d Beck,
2007), such th a t 86% o f th e E u ro p ea n coast is at h igh o r m o d erate
risk for u nsustainable coastal c o n stru c tio n a n d developm ent
(B ryant et al., 1995; EEA, 1999). A n established EU N atura2000
n e tw o rk o f p ro tec te d areas is aim ed at conservation o f the m o st
th rea te n e d species a n d h abitats, yet m an y o f these species a n d h a b i­
tats are still in jeo p a rd y (S undblad et al., 2011). O ften, d eg rad atio n
has m odified coastal h ab itats to th e degree th a t th ey n o longer fulfil
nursery, feeding, o r rep ro d u ctiv e functions (Beck et al., 2001; W orm
© 2013 In tern a tio n a l C ouncil for th e E x ploration o f th e Sea. P ublished b y O xford U niversity Press. All rights reserved.
F or Perm issions, please em ail: journals.perm issions@ oup.com
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Ecological value of coastal habitats for commercially
and ecologically important species
649
Ecological value o f coastal habitats
Coastal habitats
C oastal habitats are defined in various ways b y EU countries; we
used several sources o f in fo rm a tio n regarding coastal h abitats to
guide o u r d e finition. A general d e fin itio n o u tlin e d in th e ICES
Science P lan states: “C oastal-zone h a b ita t includes highly p ro d u c t­
ive estuaries a n d bays, w hich are essential n u rse ry g ro u n d s for a
n u m b e r o f co m m ercial a n d recreational fish species a n d h o m e to
a n u m b e r o f invertebrates (e.g. clam s, crabs). As well, this h a b ita t
is critical to successful m aricu ltu re o p e ratio n s” (ICES, 2008). This
d e fin itio n was a m e n d ed using th e follow ing sources to derive classi­
fications o f various h abitats in clu d e d in o u r review: th e H abitats
D irective (9 2 /4 3 /E E C ), M arine Strategy F ram ew ork D irective
(2 0 0 8 /5 6 /E C ) (M SFD ), W ater Fram ew ork D irective (2 0 0 0 /6 0 /
EC), a re p o rt o f the ICES W orking G ro u p o n M arine H a b ita t
M ap p in g (ICES, 2010), a n d a recent scientific review (A iroldi a n d
Beck, 2007; Table 1). For fu rth e r details a n d for a d d itio n al
in fo rm a tio n regarding th reats to th e various habitats, consult
A iroldi a n d Beck (2007), w hose h a b ita t descriptions we have
a d ap ted below.
Coastal tidal w etlands and saltm arshes
T he coastline o f E urope is characterized b y estuaries, lagoons,
a n d in te rtid a l bays in te rtw in ed w ith saltm arshes a n d irregularly
flooded w etlands (A iroldi a n d Beck, 2007). C oastal w etlands are
highly pro d u ctiv e a n d provide nursery, feeding, a n d spaw ning
g ro u n d s for com m ercially a n d ecologically im p o rta n t fish, shellfish,
a n d bird s. C oastal w etlands are patchw orks o f sand flats, m u d flats,
tidal creeks, a n d saltm arshes. Saltm arshes are low coastal grasslands
w ith stru c tu ra lly com plex vegetation a n d distinctive patches th a t are
regularly flooded b y tidal flow a n d w hich replace m angroves in te m ­
perate a n d A rctic regions.
Shallow vegetated habitats
T he key vegetated habitats in shallow w ater include seagrass
m eadow s a n d m acroalgal beds. Seagrasses are rhizom atous, clonal,
m arin e plants fo rm in g beds th a t provide food a n d refuge for m an y
com m ercial species a n d w hich enhance n u trie n t cycling, w ater
quality, a n d sedim ent dynam ics (D uarte, 2002; A iroldi a n d Beck,
2007). Seagrasses can colonize a variety o f coastal habitats from estuarine to m arine, subtidal to intertidal, a n d sedim entary to rocky.
Several seagrass species o ccu r along the E uropean coastline, in clu d ­
ing the natives Zostera m arina, Z. noltii, R uppia m aritim a, R. cirrhosa,
a n d Cymodocea nodosa.
M acroalgal beds are m ad e u p o f erect b ro w n a n d red m acroalgae,
such as kelps a n d fucoids, w hich are ecosystem engineers b y form ing
com plex, p ro d u c tiv e h abitats utilized b y vario u s com m ercially and
recreationally exploited species. M acroalgae colonize shallow h a rd
substrates such as rock, b oulders, cobble, a n d artificial structures
fro m in te rtid a l to subtidal h abitats as deep as 30 m (A iroldi and
Beck, 2007). T he d o m in a n t m acroalgae o f th e n o rth w estern
E u ro p ean coastline include L am inaria hyperborea, L. digitata,
Saccharina latissima, Fucus serratus, a n d Alaria esculenta.
Biogenic reefs and beds
B iogenic reefs a n d beds are th ree -d im e n sio n al stru c tu re s created b y
oysters, m ussels, o r polychaete w orm s. S ubsequent generations
o ften attach to o ld er individuals, fo rm in g d istin c t clusters. O yster
species include the native E uropean flat oyster (Ostrea edulis) and
Table 1. Classification of coastal habitats of im portance to exploited species in the eastern N orth Atlantic O cean and M editerranean Sea.
Class
Coastal w etlan d s/m arshes
Shallow vegetated
Biogenic reefs and beds
M ariculture beds
Soft b o tto m
Hard structure
O pen water
Habitat
Coastal w etlands
Saltm arshes
Seagrass beds
Kelp beds
Benthic algae
O yster reefs
Mussel beds
W orm reefs
Cockle beds
Maerl
O yster beds
Mussel beds
Intertidal flats
Subtidal soft bo tto m
Rocky shore
Artificial substrates
Shallow open w ater
Description
Patchwork of sand flats, m ud flats, and saltm arshes
Low coastal grassland frequently flooded by tidal flow
Beds of rooted, flowering plants (four species)
Kelps, fucoids, and o th er complex, erect macroalgae
Bushy, flat, or crustose algae
Three-dim ensional structures created by oysters, mussels, or m arine
polychaete w orm s spanning intertidal to subtidal areas
Aggregations of buried cockles in shallow s a n d /m u d flats
Coralline algae growing in beds in the sublittoral habitats
As above, three-dim ensional structures of oysters and mussels form ed
by aquaculture operations in intertidal an d subtidal areas near th e coast
Intertidal m ud and sand flats
Subtidal m ud, sand, and mixed sedim ents
Intertidal and subtidal rock, boulders, and cobble
M anm ade structures co nstructed of hard substrates
W ater dep th s shallower th an 30 m b ut n o t directly next to th e coast
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
et al., 2006). T his has consequences for several ecosystem services
p rovided b y these coastal habitats. It has even been estim ated th at
th e ecosystem goods a n d services p rovided b y coastal habitats,
such as seagrass beds, in te rtid a l habitats, a n d saltm arshes, are a p p re ­
ciably h igher per u n it area th a n th o se p rovided b y terrestrial habitats
(C ostanza eta l., 1997).
A lthough th e influence o f coastal habitats o n p a rticu la r d e m o ­
graphic rates such as survival, grow th, a n d re p ro d u c tio n has been
d e m o n stra ted (C h ích aro et al., 1998; A llain et al., 2003; Kostecki
et al., 2011; M a rtin et al., 2011; Vasconcelos et al., 2013), the
degree to w hich coastal h abitats are im p o rta n t for exploited
species at the p o p u la tio n level has n o t b e en quantified. M an y
species rely o n different coastal h ab itats to fulfil th e ir life cycle; th ere ­
fore, h a b ita t q uality a n d c onnectivity are considered essential c h a r­
acteristics o f coastal ecosystem s (L ipcius etal., 2008). T hus, there is a
critical need to define the integ rated value o f coastal ha b ita ts to
p o p u la tio n abu n d an ce, a n d ultim ately fishery yield o f exploited
species (ICES, 2008). W e review ed th e literature, exam ining links
betw een coastal h abitats a n d exploited species o r species im p o rta n t
in th e foodw eb o f exploited species, to provide the fo u n d a tio n and
justification for q u antifying the p ro d u c tio n value o f coastal habitats
for exploited species a n d subsequently to integrate h a b ita t quality in
stock assessm ent a n d ecosystem -based fishery m anagem ent.
R. D. Seitz et al.
650
Mariculture beds and aggregations
A quaculture represents a grow ing c o n trib u to r to the p ro d u c tio n o f
aquatic food w orldw ide (w w w .fao.org). In the EU, a q u acu ltu re p r o ­
d u c tio n is a n im p o rta n t econom ic activity in m a n y coastal a n d estu arin e areas. In term s o f p ro d u c tio n , shellfish farm ing represents
the m o st im p o rta n t sector (B ostock e ta l., 2010). Shellfish farm ing
is p rim a rily based o n bivalves th a t are b o rn in the w ild (i.e.
n a tu ra l spatfall) a n d rely o n food (e.g. p h y to p la n k to n ) provided
b y the n a tu ra l e n v iro n m en t in w hich th ey are c ultured. Two m ain
categories o f farm ing are practiced in the EU: suspended o r offb o tto m cu ltu re a n d b o tto m cu ltu re (M cK indsey et al., 2011).
S uspended cu ltu re is used in deeper, su b tid al w aters a n d includes
suspended ropes a n d longlines from floating rafts for m ussel a n d
o th e r shellfish species. T his tech n iq u e was developed to take ad v an ­
tage o f spatfall locations as well as areas o f good w ater quality a n d
food availability. O ff-b o tto m cu ltu re is m ain ly c arried o u t in in te r­
tidal areas w ith m acro tid al regim es, w ith o ff-b o tto m trays for
oysters a n d poles o r stakes (b o u ch o ts) for m ussels. B o tto m shellfish
cu ltu re is a type o f cu ltu re w here juvenile o r a d u lt anim als are placed
o r relayed o n the b o tto m for on-grow ing. T his type o f c u ltu re is
m ain ly c o n d u cted in shallow coastal a n d estuarine areas, b o th in te r­
tidal a n d shallow subtidal.
M ussels are the m ain shellfish species p ro d u c e d in E urope
(Sm aal, 2002). Two species are being cultured: th e blue m ussel
(M. edulis) a n d th e M ed iterran ean m ussel (Aí. galloprovincialis).
E u ro p ean aq u acu ltu re o f m ussels relies alm ost entirely o n n a tu ra l
spatfall. Besides m ussels, tw o species o f oysters are c ultured: the
Pacific oyster (C. gigas) a n d the native E u ro p ean flat oyster (O.
edulis). O f th e tw o oyster species, th e Pacific oyster d o m in ates in
m aricu ltu re o perations. O th e r shellfish cu ltu red in E urope
include a n u m b e r o f species o f clam s, scallops, a n d abalones.
U nvegetated soft bottom , hard structure, and open w ater
These h abitats are w idespread in w estern E u ro p ea n w aters a n d
include in te rtid a l a n d shallow su b tid al m u d flats, sand flats (exclu­
sive o f coastal tidal w etlands), b o tto m s o f m ixed sedim ents, a n d
h a rd -b o tto m h ab itats su ch as rock, b oulders, a n d cobble.
M an m ad e h a rd stru ctu res include those used as artificial reefs a n d
e ro sio n -co n tro l stru ctu res th a t can also provide valuable habitat.
O p e n w aters in the coastal zone are defined as those shallow er
th a n 30-m d e p th , b u t are n o t directly next to the coast.
Exploited species
C om m ercial species from the N ortheast Atlantic are poorly repre­
sented in the literature covering quantitative habitat assessments or
habitat-specific dem ographic rates in coastal areas (Vasconcelos
et al., 2013). It was, therefore, o f interest to establish to w hat degree
com m ercial species use coastal habitats. The present review was
focused o n the species for w hich ICES gives advice (hereafter
“ICES-advice species”), directing this sum m ary com pilation to im ­
p o rtan t stocks for ICES M em ber C ountries (i.e. Belgium, D enm ark,
Estonia, Finland, France, Germany, Iceland, Ireland, Latvia,
Lithuania, the Netherlands, Norway, Poland, Portugal, Russia, Spain,
Sweden, and the UK; US and C anadian fish stocks are n o t included
in the advice, though these are ICES M em ber Countries) a n d to taxa
for w hich inform ation o n the influence o f coastal habitats could be
incorporated in future ecosystem -based advice.
ICES gave advice for 59 taxa in 2012 (ICES, 2012; Table 2). Stocks
w ith full analytical assessm ent w ere inclu d ed to g eth er w ith datap o o r stocks o r species for w hich o nly p re ca u tio n a ry advice is
given. To increase th e cover o f invertebrate species, we investigated
a n u m b e r o f m olluscs a n d crustaceans th a t are im p o rta n t e co n o m ­
ically o r ecologically, specifically for ICES M em ber C ountries.
Methods
Literature review
W e com piled relevant scientific literatu re o n h a b ita t use o f the
IC E S-relevant species a n d o f a n u m b e r o f a d d itio n al invertebrates
w ith high landings in the ICES A rea o r th a t are o f ecological im p o rt­
ance. T he searches w ere m ad e using G oogle Scholar, p rim a rily by
c o m b in in g species n a m e + h a b ita t fu n c tio n (spaw ning, nursery,
feeding, m ig ratio n ). In cases w here n o m atches w ere fo u n d , we
m ad e searches b y species n a m e + h a b ita t n am e a n d finally by
h a b ita t n a m e + “fish” o r “invertebrates” for h abitats po o rly re p re ­
sented in th e o riginal search. D e p th ranges for v arious species were
o b tain e d fro m FishBase (Froese a n d Pauly, 2013). W e also recognize
th a t shellfish a q u acu ltu re is gaining im p o rta n ce a n d has th e p o te n ­
tial to greatly influence coastal b e n th ic habitats; thus, we exam ined
th e influence o f shellfish a q u acu ltu re o n these habitats.
Habitats and habitat function
C oastal h abitats w ere as defined above, b u t m odifications h a d to be
m ad e to this classification to a cc o m m o d ate th e lack o f detailed
h a b ita t descriptions in the literatu re a n d th e p o o r re p resen tatio n
o f som e habitats in fish studies. W e evaluated h a b ita t use o f c o m ­
m ercially im p o rta n t fish species a n d invertebrates b y exam ining
fo u r different ecological h a b ita t functions: spaw ning, nursery,
feeding, a n d m igration. T he categorization was m ain ly based o n
papers referring to these functions, b u t also, in som e instances, o n
o u r conclusions referring to th e d e finitions o f fu n ctio n s in Table 1.
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
the in tro d u ced Pacific oyster ( Crassostrea gigas), w hich is easier to cul­
tivate th a n the native oyster. Blue m ussel (M ytilus edulis) beds are also
c o m m o n along the N ortheast A tlantic coast. Generally, the m ussel
bed co m m u n ity is m o re species rich a n d contains different species
th a n the su rro u n d in g soft sedim ent hab itat (C o m m ito et al., 2008;
B uschbaum et al., 2009; Ysebaert et al., 2009). T hree-dim ensional
structures are also co nstructed b y m arin e polychaete w orm s in the
fam ily Sabellariidae, p rim arily Sabellaria alveolata a n d Lanice conchi­
lega in E uropean waters. These structures consist o f sedim ents co n so ­
lidated b y a m u co p ro tein cem ent pro d u ced by the w orm s. Biogenic
reefs occur in the intertidal to subtidal zones.
Cockle beds are com posed o f aggregations o f cockles buried a few
centim etres below the surface in shallow sand, m ud, and gravelly
flats from the intertidal to subtidal zones. The m ost w idespread is
the edible, c o m m o n cockle (Cerastoderma edule), though another
cockle (C. glaucum) can also be locally abundant. Cockles can occur
in extrem ely dense aggregations reaching m ore th an 1000 ind. n V 2.
M aerl (a rh o d o lith b ed) encom passes various species o f u n ­
attached, c rust-form ing, calcareous re d algae th a t can fo rm su b sta n ­
tial beds o f live a n d dead m aterial, n o t unlike coral reefs a n d oyster
reefs, a n d w hich can serve as n u rse ry h a b ita t (Steller a n d
C áceres-M artínez, 2009). T he m ain m ae rl-fo rm in g E u ro p ean
species are P hym atolithon calcareum, L ithotham nion corallioides,
a n d I . glaciale. M aerl beds occu r from th e surface to 100 m in
d ep th , th o u g h m o st are at 2 0 -3 0 -m d epths. P hym atolithon calcar­
eum form s brittle, p u rp le-p in k , b ra n ch e d stru ctu res th a t look
m o re like sm all corals th a n algae, a n d w hich grow as spherical
n odules at sheltered sites o r as twigs o r flattened m edallions at
m o re exposed sites. M aerl is a n im p o rta n t h a b ita t for m an y
species a n d is vulnerable to dam age fro m traw ling a n d dredging.
Coastal habitat type
Species
Com m on nam e
Seagrass
Intertidal soft Subtidal soft
b ottom
b ottom
Kelp
Shallow
open w ater
Saltmarsh
Mussel
beds
Macroalgae
Rocky
shore
Coastal
Depth range
(m )
N, F
Yes
Yes
1 0 -1 5 0
0 -7 0 0
References
A m m o d ytes m arinus
Anguilla anguilla
Sandeel
Eel
Aphanopus carbo
Black scabbard
fish
Greater silver
sm elt
A lfonslnos/
G olden eye
perch
Tusk
Boarfish
2 0 0 -1 700
Holland et al. (2005)
M orlarty and Dekker
(1997); Pihl and
W ennhage (2002);
Cattrljsse and Hampel
(2006); Pihl et al.
(2006); Bergström et al.
(2011)
Swan et al. (2003)
1 4 0 -1 440
M agnûsson (1996)
1 0 0 -1 000
Aníbal eta l. (1998)
Leafscale guiper
shark
Portuguese
dogfish
Basking shark
Red gurnard
1 4 5 - 2 400
FAO (1990)
Blanchard and
Vanderm elrsch (2005)
Verisslmo et al. (2012)
1 5 0 - 3 700
Verisslmo et al. (2011)
Argentina silus
Beryx spp.
Brosme brosme
Capros aper
Centrophorus
squam osus
Centroscymnus
coelolepis
Cetorhinus m axim us
Chelidonichthys
cuculus
Chelidonichthys
spinosus
Clupea harengus
N, F
S, N, F
N
N, F
F
M
N, F
N, F
1 8 - 1 000
4 0 -7 0 0
F
Yes
Spiny red gurnard
Herring
Coryphaenoides
rupestris
Dalatias licha
Dicentrarchus labrax
Roundnose
grenadier
Kltefin shark
European sea bass
Engraulis
encrasicolus
Eutrigla gurnardus
Anchovy
0 - 2 000
1 5 -4 0 0
Ecological value of coastal habitats
T able 2. Coastal habitat use of commercially im portant fish species for which ICES gave advice in 2012.
Slms (2008)
Lopez-Lopez et al. (2011)
2 5 -6 1 5
S
N, F
S
S
S
Yes
0 -3 6 4
Rajasllta et al. (1989);
N o ttestad et al. (1996);
Pihl and W ennhage
(2002); Polte and
Asmus (2006); Jensen
et al. (2011)
1 8 0 - 2 600
N
N
N
Yes
3 7 - 1 800
1 0 -1 0 0
Yes
0 -4 0 0
Grey gurnard
Jennings an d Pawson
(1992); Laffallle et al.
(2001)
M otos et al. (1996); Drake
et al. (2007)
1 0 -3 4 0
Continued
HOZ ‘EI IsnSny uo say eag .ioj jsuj spirepaipafvj qiy je /§jo s[eiuiiofpjojxo srarsa3i//:dtti[ uio.ij papeopiMOQ
en
T able 2. Continued
Coastal habitat type
Species
Com m on nam e
Cadus m orhua
Cod
Glyptocephalus
cynoglossus
Hoplostethus
atlanticus
Lamna nasus
Lepidorhombus
boscii
Lepidorhombus
whiffiagonis
Limanda lim anda
Witch
Lophius budegassa
Black-bellied
anglerfish
Anglerfish
Capelin
Haddock
Lophius piscatorus
M allotus villosus
M elanogram mus
aeglefinus
Merlangius
merlangus
Merluccius
merluccius
Micromesistius
poutassou
Microstomus kitt
Molva dypterygia
Molva molva
Mullus surm uletus
Seagrass
Intertidal soft Subtidal soft
bottom
bottom
N
N
Kelp
Shallow
open w ater
Saltmarsh
Mussel
beds
Macroalgae
N
N, F
Rocky
shore
N
Depth range
Coastal
(m )
References
Yes
0 -6 0 0
Uzars and Pllkshs (2000);
Pihl and W ennhage
(2002); N orderhaug
et al. (2005)
1 8 - 1 570
Orange roughy
1 8 0 -1 809
Porbeagle
Fourspot megrim
0 -7 1 5
7 -8 0 0
Megrim
1 0 0 -7 0 0
Dab
W hiting
N
N
Yes
0 -1 0 0
Bolle et al. (1994); Gibson
et al. (2002)
2 0 - 1 000
S
N
S
N
N
Yes
2 0 - 1 000
0 -7 0 0
1 0 -2 0 0
Yes
0 -1 0 0
Hake
3 0 - 1 000
Blue whiting
1 5 0 -1 000
Lemon sole
Blue ling
Yes
1 0 -2 0 0
1 5 0 -1 000
1 0 0 -1 000
5 -1 0 0
Ling
Striped red m ullet
N
N
Nephrops norvegicus
Pagellus bogaraveo
Pandalus borealis
Phycis blennoides
Platichthys flesus
Norway lobster
Red sea bream
N orthern prawn
Greater forkbeard
Flounder
N
N, F
N
Yes
2 0 -8 0 0
<700
2 0 - 1 000
1 0 -8 0 0
0 -1 0 0
Pleuronectes platessa
Plaice
N
N, F
N
Yes
0 -1 0 0
H OZ £1 Jsn S n y u o s a y e a g .ioj jsuj spue[jai[ja[\j q iy je /§ jo s [e u in o rp jo jx o sm rsaai//:dm [ kio .ij papeojuM O Q
Penton et al. (2012)
Plhl and W ennhage
(2002)
Santos and M ontelro
(1997)
Santos and M ontelro
(1997); Rogers et al.
(1998); M athleson
et al. (2000)
Cattrljsse and Hampel
(2006); Florin et al.
(2009)
Glbson (1999); Cattrljsse
and Hampel (2006)
Pollack
N
N
Yes
0 -2 0 0
Pollachius virens
Salthe
N
N
Yes
0 -3 0 0
Reinhardtius
hippoglossoides
Salmo salar
Salmo trutta
G reenland halibut
Salmon
Sea tro u t
Sardina pilchardus
Sardine
Scomber scombrus
Mackerel
Scophthalm us
m axim us
T urbot
S, N
Yes
Scophthalm us
rhom bus
Sebastes m arinus
Sebastes mentella
Brill
S, N
Yes
Golden redfish
Beaked redfish
Solea solea
Sole
N, F
S,M
Yes
<60
Sprattus sprattus
Sprat
N,
N, F
Yes
<150
Squalus acanthias
Trachurus picturatus
Spurdog
Blue jack
mackerel
Horse mackerel
Norway pout
M
F
M
F
M
F
M
F
1 - 2 000
Pihl et al. (1994);
N orderhaug et al.
(2005)
Pihl and W ennhage
(2002); N orderhaug
et al. (2005)
G odo and Haug (1989)
Yes
Yes
0 -3 0
0-10
M cCorm ick et al. (1998)
Pihl and W ennhage
F
Yes
1 0 -1 0 0
N. M
Yes
0 -1 0 0
Elliott an d DeWallly
(1995)
Eltlnk (1987); Jamieson
and Smith (1987)
Gibson (1973); 0 le et al.
(1997); Iglesias et al.
(2003)
Gibson (1973,1994);
C hanet (2003)
Plkanwskl et al. (1999)
Plkanwskl et al. (1999);
Roques et al. (2002)
Dorel et al. (1991);
Koutslkopoulos et al.
(1991); Cabrai (2000);
C rloche et al. (2000);
Laffallle et al. (2000)
Elliott et al. (1990);
Laffallle et al. (2000);
Voss et al. (2003);
Gorokhova et al.
(2004); Baumann et al.
(2006)
M
F, M
M
F
M
F
(2002 )
Trachurus trachurus
Trisopterus esmarkii
<70
5 -5 0
5 0 -3 0 0
3 0 0 -1 400
Ecological value of coastal habitats
Pollachius pollachius
<200
<300
Yes
1 0 0 -1 000
5 0 -3 0 0
Pihl et al. (2006)
The function of coastal habitats for species was divided into (S) spawning area, (N) nursery ground, (F) feeding area, and (M) migration route. Coastal habitat types constitute a subset of the habitats in Vasconcelos et al.
(2013) for which there was information on species habitat use. Depth ranges were collated from FishBase.
653
HOZ £1 IsnSny uo say eag .ioj jsuj spire[jat[ja[\j qig je /§jos[eiunorpjojxosmrsaai//:dm[ uio.ij papeojuMog
654
R. D. Seitz et al.
(i) Spawning: records o f ripe adults, observ atio n o f spaw ning, or
th e presence o f new ly spaw ned eggs;
(ii) N ursery: reference to the c o n ce n tra tio n o f juvenile stages o r at
least th e presence o f juveniles;
(iii) Feeding: th e use o f habitats b y adults as feeding g ro u n d s o r at
least th e presence o f adults n o t related to spaw ning; a n d
(iv) M igration: m ain ly refers to the directio n al m o v em en t o f diad ro m o u s species.
C atches o f species using coastal habitats a n d ICES-advice species
w ere th e n related to th e to ta l catch in th e N o rth e ast A tlantic using
d a ta from ICES catch statistics for 2010 (h ttp ://w w w .ic e s.d k /
fish / CATCHSTATISTICS.asp).
O u t o fth e 59 ICES species investigated, 26 species (44% ) were consid­
ered to use coastal habitats. N one o fth ese 59 species seem ed to be resi­
d e n t in a single coastal habitat, a n d for the large m ajority o f species,
the life cycle also had a non-coastal co m p o n e n t (Table 2). In addition,
a n u m b e r o f species used m ore th an one type o f coastal habitat.
Overall, the nu rsery function was the m ost prevalent function, o ccur­
ring in 30% o f the ICES species, followed b y feeding grounds for 20%,
spaw ning areas for 10%, a n d m igration routes for 8% (Figure 1).
In o u r review, representatives o f ICES-advice species utilized
m o st h abitats th a t we investigated, a n d all habitats except kelp, salt­
m arshes, a n d m ussel beds su p p o rte d all th e fo u r functions for at
least one species (Figure 2). S ubtidal soft b o tto m was th e hab itat
used as spaw ning a n d n u rse ry areas b y the largest p ro p o rtio n o f
species, a n d in te rtid a l soft b o tto m was also used heavily as n u rsery
grounds. T he m o st prevalent h a b ita t for feeding a n d m ig ra tio n
a m o n g th e ICES species was shallow o p e n w ater, th o u g h subtidal
soft b o tto m was also used b y m an y species for feeding (Figure 2).
In a d d itio n , o u r literature review show ed th a t th ere is a specific
lack o f in fo rm a tio n o n fish from com plex h a rd b o tto m hab itat
types, inclu d in g kelps a n d m acroalgae, p articu larly in E urope.
Coastal habitat use by Invertebrates
A considerable n u m b e r o fco m m ercial invertebrates use coastal habi­
tats. ICES gives advice for o nly tw o invertebrate species— N orw ay
35 --------------------------------------------------------------------------------------
+*
cu
5
«
O
30 ■
---------
25 ■
20 ■
------------
d>
M
=
15 ■
Í
2
o
10 ■
---------
--------
I-
5 ■
0 ------------— i— ---- — i— ------ — i— ------ — i— ----------S paw ning
N ursery
F eeding
M ig r a tio n
Habitat
Figure 1. Percentage (%) of ICES-advice fish species using coastal
habitats for spawning, as nursery grounds, for feeding, and for
migration.
Catches o f ICES-advice species using coastal habitats
T otal landings o f fish a n d invertebrates re p o rte d w ith in the ICES
A rea w ere estim ated to be 8 514 820 t for 2010. H e rrin g ( Clupea har­
engus) co m p rised th e highest to n n ag e o f catch a n d the largest p e r­
centage o f to ta l catch in the N o rth e ast A tlantic (~ 2 3 % ); this
species utilized coastal h abitats fo r n u rse ry gro u n d s, spaw ning,
a n d feeding (Tables 2 a n d 4). C o d ( Gadus m orhua) a n d m ackerel
(Scomber scombrus) represented th e next highest tonnages a n d p e r­
centages, to g eth er a cc o u n tin g for over 20% o f to ta l catch (Table 4).
T hey utilized coastal habitats for nursery, feeding, a n d m igration
areas (Table 2). Blue w hiting (Micromesistius poutassou), sprat
(Sprattus sprattus), capelin (M allotus villosus), sandeel (A m m odytes
m arinus), had d o ck (M elanogram m us aeglefinus), saithe (Pollachius
virens), a n d blue jac k /h o rse m ackerel ( Trachurus spp.) ro u n d e d o u t
the to p ten species in term s o f tonnage, w ith seven o f these ten
species utilizing coastal habitats (Table 4).
T he species associated w ith coastal h a b ita ts m ad e u p 71% o f the
to ta l landings a n d 77% o f th e cum ulative landings o f ICES-advice
species in th e N o rth e ast A tlantic (Table 4). A lthough the N orw ay
lobster is a com m ercially im p o rta n t invertebrate species in E urope
a n d rep resen ted th e largest percentage o f to ta l ICES catch o f any in ­
vertebrate, it acco u n ted for less th a n 1% o f th e to ta l fishery catch in
th e N o rth e ast A tlantic (Table 4).
Influence o f shellfish aquaculture on benthlc habitats
A lthough there are m a n y a n th ro p o g e n ic influences o n coastal h a b i­
tats, shellfish a q u acu ltu re is a m ajo r o n e o f increasing concern.
P otential positive a n d negative en v iro n m en tal effects o f different
shellfish aq u acu ltu re practices are w idely described in the scientific
a n d technical literature (e.g. Kaiser e ta l., 1998; Newell, 2004; B orja
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Results
Coastal habitat use by ICES-advice species
lobster (Nephrops norvegicus) a n d n o rth e rn sh rim p (Pandalus bor­
ealis). O ne reason for this m ay be th a t m an y com m ercially im p o rt­
a n t invertebrates are less m obile th a n fish, such th a t th e local
p o p u latio n s are, therefore, m anaged nationally. W e chose to d o a
close e x am in atio n o f coastal h a b ita t use for com m ercially im p o rta n t
invertebrates th a t h a d a su b stan tial percentage o f fishery landings in
th e ICES Area, as well as for a n u m b e r o f species o f p a rticu la r interest
d u e to th e ir m ajo r c o n trib u tio n to o th e r fishery landings in the
A tlantic (e.g. Callinectes sapidus) o r as im p o rta n t p rey species (e.g.
M acom a balthica) for o th e r com m ercially im p o rta n t species
(Table 3).
O f the 12 invertebrate species exam ined, all used coastal h a b ita t
d u rin g som e phase o f th eir life h isto ry (Table 3). All h abitats except
kelp a n d saltm arsh w ere used b y several o f the invertebrate species
we exam ined. Shallow o p e n w ater was th e h a b ita t m o st c o m m o n ly
used b y invertebrates for spaw ning, w hereas in te rtid a l a n d su btidal
so ft-b o tto m h abitats w ere used b y th e largest p ro p o rtio n o f in v erte­
brates as nurseries. S ubtidal so ft-b o tto m habitats w ere used m ost
c o m m o n ly for feeding. M ost o f th e coastal habitats investigated,
except kelp, w ere used b y invertebrates for th e n u rse ry fu n c tio n
(Figure 3).
O f th e coastal habitats investigated, shallow su b tid al a n d in te r­
tidal h abitats w ere th e m o st c o m m o n ly used b y invertebrates, w ith
1 6 -2 5 % o f the invertebrate species we investigated using these
tw o h abitats for spaw ning, 50% o f species using these habitats for
n u rse ry grounds, a n d 2 5 - 5 8 % o f species using these h abitats for
feeding (Figure 3). Shallow o p e n w ater habitats w ere used n o t
o nly for invertebrate spaw ning, b u t also for n u rse ry g ro u n d s a n d
feeding. R ocky shores w ere also c o m m o n ly u sed for feeding ( 16%
o f species) o r as n u rse ry grounds.
655
Ecological value o f coastal habitats
Spaw ning
Nursery
M i g r a t io n
(d )
P P P . I^
¿Si
*0«
■
*
/■
✓ ^
\
*
c f?
4
s-
\
&
H abitat
Figure 2. Relative contribution (%) o fth e different coastal habitats for the main functions (spaw ning nursery, feeding m igration) identified am ong
th e ICES-advice fish species th a t use coastal habitats (26 species).
etal., 2009; F orrest etal., 2009; Y sebaert etal., 2009; M cK indsey et al.,
2011; Shum way, 2011; C ran fo rd et al., 2012). E nv iro n m en tal c o n ­
cerns are related to ho w shellfish c u ltu re interacts w ith o r controls
basic ecosystem processes (C ran fo rd e ta l., 2012). T he effects o f dif­
ferent aq u ac u ltu re system s d e p en d o n various factors, such as the
local h y d rographic c o n d itio n s, th e se d im e n tary h a b ita t in w hich
a q u acu ltu re occurs, the type o f cu ltu red organism s, the cu ltu re
a n d p ro d u c tio n m eth o d s, a n d m an a g em e n t practices (H en d erso n
et al., 2001). T he effects are also site-specific a n d d e p en d largely
o n the local e n v iro n m en ta l co n d itio n s (Read a n d Fernandes,
2003). T he sensitivity o f the ecosystem , the h abitats in w hich
c u ltu re practices occur, a n d th e assim ilative capacity o f the su r­
ro u n d in g en v iro n m en t are key to d e te rm in in g th e m ag n itu d e a n d
significance o f th e im p a c t (C ra n fo rd et al., 2012; B unting, 2013).
Shellfish p o p u latio n s rely o n the n a tu ra l availability o f n u trie n ts
a n d algae for th eir grow th (Sm aal a n d V an Stralen, 1990; D am e,
1996). H ighly pro d u ctiv e areas are preferred, such as shallow bays
a n d estuaries (N unes etal., 2003). A healthy ecosystem is, therefore,
o f u tm o s t im p o rta n ce for shellfish aquaculture. T hese areas are also
o ften rich in b iodiversity a n d act as im p o rta n t n u rse ry g ro u n d s for
fish a n d crustaceans a n d feeding areas for b ird s (Sequeira et al.,
2008). Because o f this, m an y o f these areas are in te rn atio n ally p ro ­
tected a n d are p a rt o f the E u ro p ean N atura2000 netw ork. T his can
lead to conflicts w ith shellfish o perations, as was the case in the
N etherlands. P ro p e r p lan n in g a n d lo catio n o f activities should
proceed in a sustainable m a n n e r a n d a t sustainable levels, according
to th e carrying capacity o f p a rticu la r areas. Recently, focus is n o t
solely o n carrying capacity in term s o f th e m ax im u m sustainable
yield (MSY) o f th e bivalve culture, b u t also o n p o ten tial changes
in ecosystem stru c tu re a n d fu n c tio n in g a n d ecological variability
over different spatial a n d tem p o ral scales (C ra n fo rd et al., 2012).
A n ecosystem -based m an ag em en t p olicy th a t balances th e different
needs is in th e lo n g -te rm interest o f coastal co m m u n itie s a n d sus­
tainable developm ent o f coastal resources.
Coastal habitat use by individual species
To provide concrete exam ples o f the ecological value o f coastal h a b i­
tats for fish a n d invertebrates, we highlight a selection o f c o m m e r­
cially im p o rta n t species fro m th e ICES A rea a n d describe th eir
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
F eeding
Table 3. C oastal h a b ita t use by se lected com m ercially o r ecologically im p o rta n t invertebrates.
Coastal habitat type
Species
Com m on
nam e
Crangon
crangon
C om m on
shrim p
Ostrea edulis
Callinectes
sapidus
Homarus
gam m arus
Oyster
Blue crab
M acom a
balthica
Baltic clam
Cancer pagurus
Edible crab
Palaemon
serratus
Placopecten
magellanicus
C om m on
prawn
A tlantic
sea
scallop
Ocean
quahog
Blue
mussel
Arctica
islandica
Mytilus edulis
Cerastoderma
edule
Buccinum
undatum
Seagrass
Intertidal
soft
b ottom
Kelp
Shallow
open
water
Saltmarsh
N,F
N, F
F
S, M
N
N
N
N
S
N
N, F
S
S, N, F
S, N, F
S
N
F
M
N, F
N
European
lobster
C om m on
cockle
W helk
Subtidal
soft
b ottom
N
F
F
Oyster
Reef
S, N, F
N
Mussel
beds
N
Macroalgae
Rocky
shore
Coastal
N
N, F
N
N
S, N, F
S, N, F
S, N, F
S, N, F
S
Pandian (1970); Nichols an d Fawton
(1978); Howard an d Bennett (1979);
Tully and Céidigh (1987);Jensen etal.
(1994); W ähle and Steneck (1991)
Bachelet (1980); Olafsson (1986);
Beukema and de Vlas (1989);
Arm onies an d Hellwig-Armonies
(1992); Hiddink (2002)
Brown and Bennett (1980); Bennett and
Brown (1983); Haii et al. (1993);
Sheehy and Prior (2008)
Berglund (1982); C uerao and Ribera
(1996, 2000)
M acD onald and T hom pson (1985);
Packer et al. (1999); Hart (2006)
T hom pson et al. (1980)
S,N, F
S, N, F
References
Pandian (1970); Nichols an d Fawton
(1978); Howard an d Bennett (1979);
Tully and Céidigh (1987); W ähle and
Steneck (1991); Jensen et al. (1994);
Cattrijsse et al. (1997); Polte et al.
(2005)
Fauney et al. (2002)
Fipcius et al. (2008)
S, N, F
S, N, F
S, N, F
S, N, F
Fintas and Seed (1994); Prins and Smaal
(1994); Hilgerloh (1997); W alter and
Fiebezeit (2003)
Boyden and Russell (1972); Seed and
Brown (1978)
Him m elm an and Hamel (1993)
The function of coastal habitats for species was divided into (S) spawning area, (N) nursery ground, (F) feeding area, and (M) migration route. Coastal habitat types constitute a subset o fth e habitats in Vasconcelos et al.
(2013) for which there was information on species habitat use.
HOZ SI Isrá^ V uo
B9§ lo j isuj spuetJ9ip9N q iq je /Sio-sjeumofpiojxosra Tsaoi//: duq raojq papeojuMOQ
657
Ecological value o f coastal habitats
70
■
Spawning
(a)
60 ■
T able 4. C a tc h es o f ICES species w ith coastal h a b ita t use (Yes, o r
N o = left blank) acco rd in g t o T able 2 a n d related to th e to ta l ca tc h
in th e N o rth e a st A tlan tic (0% ca tc h m e a n s < 0.01%).
Catch
50 ■
Species
40 ■
30 ■
20 ■
ml □
10 ■
0 ■
Nursery
sS
as
*-•
Xi
aí
x:
o
50 ■
40 ■
0)
<n
30 ■
a)
>
as
20 ■
£
10 ■
3
(b)
60 ■
n
0 ■
80
<c)
Feeding
60 ■
40 ■
20
■
□ . Ug
/ s s /* <?/«vvV*
/////
Habitat
Figure 3. Relative c o n trib u tio n (%) o f t h e d ifferen t coastal h a b ita ts for
th e m ain fu n c tio n s (spaw ning, nursery, feeding) identified a m o n g th e
in v e rte b ra te species investigated. Few in v e rte b ra te species u sed coastal
h a b ita ts for m ig ration, so th e s e are n o t d ep icted .
specific use o f coastal habitats. O th e r coastal species m ay also use
coastal habitats sim ilarly.
Plaice (Pleuronectes platessa)
Plaice o ccu r o n sandy a n d m u d d y substrata o f the E u ro p ea n shelf
fro m the B arents Sea to th e M e d ite rran e a n inclu d in g m o st o f the
% of
catch
Coastal
habitat use
1 986 630
909 008
831878
546 026
538 105
477 679
422 422
364 082
336 504
236 745
23.33
10.68
9.77
6.41
6.32
5.61
4.96
4.28
3.95
2.78
Yes
Yes
Yes
138 300
1.62
137 678
137 079
125997
83 967
63 743
59 010
58 957
55141
1.62
1.61
1.48
0.99
0.75
0.69
0.69
0.65
43 537
41 171
33 858
31 430
30 372
26 438
25 020
17 201
15 365
12 639
11 165
11 066
10 206
8 263
7191
7 094
6 892
5 396
4 731
4 593
4 405
0.51
0.48
0.4
0.37
0.36
0.31
0.29
0.2
0.18
0.15
0.13
0.13
0.12
0.1
0.08
0.08
0.08
0.06
0.06
0.05
0.05
2 958
1 172
1 152
784
634
575
490
149
118
97
88
6
0
0
0.03
0.01
0.01
0.01
0.01
0.01
0.01
0
0
0
0
0
0
0
Catches from ICES catch statistics for 2010.
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
70 ■
Herring
Cod
Mackerel
Blue whiting
Sprat
Capelin
Sandeel
Haddock
Saithe
Blue jack mackerel + horse
mackerel
Golden redfish + beaked
redfish
Boarfish
Norway p o u t
Sardine
Plaice
Pollack
Norway lobster
Hake
Anglerfish + black-bellied
anglerfish
N orthern prawn
G reenland halibut
Ling
W hiting
Tusk
Flounder
Sole
M egrim + fourspot megrim
Anchovy
Blue ling
Dab
Lemon sole
W itch
European sea bass
G reater forkbeard
Roundnose grenadier
Black scabbard fish
Striped red m ullet
T urbot
G reat silver sm elt
Red gurnard + spiny red
gurnard
Brill
Red sea bream
Eel
Salmon
Grey gurnard
Alfonsinos
Sea tro u t
Leafscale guiper shark
Portuguese dogfish
Porbeagle
O range roughy
Kitefin shark
Basking shark
Spurdog
(t)
R. D. Seitz et al.
658
Cod (C. m orhua)
C od is w idely d istrib u te d in the N o rth A tlantic a n d A rctic (Froese
a n d Pauly, 2013) a n d is fo u n d in a v ariety o f habitats, fro m the sh o re­
line do w n to the c o n tin e n ta l shelf. W h en m atu rin g , th e o p tim u m
tem p e ra tu re for cod decreases, a n d the larger fish are m ainly
fo u n d in deeper, colder w aters.
C od spaw n in pelagic h abitats usually offshore, a n d eggs a n d
larvae drift w ith c u rre n ts for m o n th s before settling to th e seabed
(Juanes, 2007). As juveniles, th ey are m ain ly fo u n d in com plex h a b i­
tats, such as seagrass beds, kelps, rocky shores, a n d gravel b o tto m s
w ith cobble a n d attached fauna, w hich p rovide shelter from p re d a ­
tio n (Pihl a n d W ennhage, 2002; L in d h o lm etal., 2004; N o rd e rh au g
et ah, 2005; Juanes, 2007). M o rta lity risk o f 0-g ro u p cod is low er in
com plex h a b ita t types th a n in sim ple habitats, suggesting th a t cod
re cru itm e n t m ay be a fu n c tio n o f h a b ita t availability (Juanes,
2007). O lder life stages o f cod are less d e p en d e n t o n specific
h a b ita t types, p ro b ab ly as a consequence o f a low er vulnerability
to pred atio n .
C od has historically b een b y far th e m o st im p o rta n t dem ersal
species o f N o rth A tlantic fisheries, a n d it c o n tin u e s to be so alth o u g h
m an y cod stocks have b een severely depleted. M ost catches are taken
in traw ls, b u t th ey are also tak en in seines, gillnets, a n d h o o k a n d line
gear. L andings o f cod w ith in the ICES A rea peaked in l9 5 6 ;in 2 0 1 0 ,
th ey w ere d o w n to 909 000 t, w hich is 40% o f th e m ax im u m h isto r­
ical catch (Table 4). A fter a few years o f low ered to ta l allowable catch
in c o m b in a tio n w ith o th e r m an a g em e n t m easures, several stocks
have n o w started to increase, w hereas others re m a in at a low level
(C ardinale e ta l., 2013).
Brown shrim p (Crangon crangon)
A n a b u n d a n t species in E u ro p ea n w aters, th e b ro w n sh rim p , also
k n o w n as the c o m m o n sh rim p , is im p o rta n t ecologically a n d as a
fishery species, especially in th e N o rth Sea. T his species tolerates
diverse e n v iro n m en ta l cond itio n s, a n d its d istrib u tio n ranges
along the E u ro p ean coast from th e W h ite Sea to M orocco, in cluding
th e M e d ite rran e a n a n d Black Seas.
A side fro m the pelagic larval stage, this species is resident in
shallow coastal areas o f 1 - 2 0 m in san d o r m u d d y sand habitats, al­
th o u g h th ere have been records o f this species fo u n d in d e p th s o f
130 m (FAO, 1999). In th e W ad d e n Sea, shallow in te rtid a l habitats
are nurseries for C. crangon from F ebruary th ro u g h June, d ep en d e n t
o n tem p eratu re. B row n sh rim p can be fo u n d in high densities in tide
pools a t low tid e ( C attrijsse a n d H am pel, 2006). T hey leave the tidal
zone a t ~ 3 0 m m in carapace length fro m July th ro u g h Septem ber,
w h en th ere is a large re cru itm e n t to the a d u lt stock. In w inter, adults
spaw n again, a n d in spring, larvae m igrate in sh o re a n d settle in the
in te rtid a l zone (K uipers a n d D apper, 1984). In th e UK, th ere are sea­
sonal m igrations betw een Severn E stuary a n d B ristol C hannel
(H e n d erso n a n d H olm es, 1987). Ecologically, th ere is evidence
th a t C. crangon is a m ajo r stru c tu rin g force for shallow, so ft-b o tto m
co m m u n ities, w here th ey are a d o m in a n t p re d ato ry species.
Crangon crangon is fished in G erm any, th e N etherlands,
D enm ark, UK, B elgium , a n d France. F or this species, th ere is n o of­
ficial ICES advice given, b u t it is o f p rim e concern, a n d th ere has
b een a n ICES W orking G ro u p for this species. In 2010, in the
N o rth Sea, th ere w ere 36 000 t landed, d o m in a te d b y G erm any
a n d th e N etherlands, a n d the stock is stable (ICES, 2011). T here is
n o m an ag em en t p lan for th e fishery, a lth o u g h th ere are som e m eshsize regulations (Innes a n d Pascoe, 2007), a n d the ICES W orking
G roup o n Crangon fisheries a n d life h isto ry has suggested th at
fu rth e r m an ag em en t sh o u ld be im p lem en ted . T he fishery cu rren tly
uses unselective gear in shallow coastal n u rse ry areas, w hich results
in excessive discards a n d dam age to th e e n v iro n m en t (ICES, 2011);
thus, the fishery could be m ad e m o re efficient.
European lobster (H om arus gam m arus)
T he E u ro p ea n lobster has a b ro a d geographic d istrib u tio n in the
eastern A tlantic from n o rth w e stern N orw ay (L ofoten Islands) to
so u th eastern Sweden a n d D en m ark , b u t possibly because o f low sal­
in ity a n d tem p e ra tu re extrem es, it is absent from th e Baltic Sea
(C h a rm a n tie r et al., 2001; FAO, 2012). Its d istrib u tio n so uthw ard
extends along th e m ain lan d E u ro p ean coast a ro u n d B ritain a n d
Ireland, to a so u th e rn lim it o f ~ 3 0 ° N latitu d e o n the A tlantic
coast o f M orocco (P ro d ö h l e ta l., 2006).
T h e re is little in fo rm a tio n o n th e j uvenile phases o fTí. gam m arus.
In E ngland, h ab itats w ith suitable crevices are so u g h t o u t, a n d in lab
experim ents, juveniles also can b u ry in fine, cohesive m u d . Early j u ­
venile stages o f th eir close relative Fi. am ericanus use cobble as th eir
m ain h abitat, a n d this h a b ita t is th o u g h t to be a dem o g rap h ic b o ttle ­
n eck to th o se p o p u latio n s (W ähle a n d Steneck, 1991). G iven th eir
sim ilar life cycles, it is reasonable to believe th a t th e sam e m ig h t
be tru e for th e E u ro p ean lobster. A dult Fi. gam m arus live o n th e c o n ­
tin e n tal shelf a n d use a ro c k crevice h a b ita t (H o w ard a n d B ennett,
1979). Gravel a n d cobble are th o u g h t to b e th e p rim e n u rse ry h a b i­
tats. M oreover, adults colonized artificial reefs in th e UK. In
England, areas w ith habitats th a t include less stru c tu re a n d fewer
large-scale o u tcro p s for ad u lts p ro d u c e lobsters o f sm aller size
th a n o th e r areas, indicatin g th e im p o rta n ce o f th e h a b ita t for
grow th (H ow ard, 1980). Larvae are spaw ned in shallow bays in
Ireland a n d display diel vertical m ig ra tio n w ith high densities in
th e n e u sto n (i.e. surface w aters) at daw n a n d d u sk (Tully a n d
C éidigh, 1987). Spaw ning begins in July, a n d a spaw ning peak
occurs in A ugust (P andian, 1970).
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
N o rth e ast A tlantic to a d e p th o f 100 m (K ottelat a n d Freyhof, 2007;
Froese a n d Pauly, 2013). Plaice are d e p en d e n t o n shallow ( 0 - 5 m )
sedim ent su b stra tu m as n u rse ry g ro u n d s d u rin g th eir early juvenile
stage, w hich is o nly a sm all fraction o f the species’ d istrib u tio n range
(G ibson, 1994). V ariation in year-class stren g th is generated d u rin g
the pelagic stages a n d subsequently d a m p e n ed d u rin g the early ju ­
venile stage (van d e r Veer, 1986; B everton, 1995). G row th rate is
negatively correlated a n d m o rta lity positively correlated w ith settle­
m e n t density, indicatin g th a t d en sity -d e p en d e n t processes are
acting in the n u rse ry g ro u n d s (P ihl et al., 2000). These nurseries
are im p o rta n t for stock dynam ics, since a re lationship betw een
n u rse ry size a n d p o p u la tio n a b u n d an c e exists, a relationship th at
has been conveyed as th e “n u rse ry size hypothesis” (R ijnsdorp
et al., 1992; v a n d e r Veer et al., 2000).
The W adden Sea is considered the largest a n d m ost im portant
nursery ground in the N o rth Sea. Spawning grounds are located such
that eggs and larvae are transported w ith prevailing currents towards
the nursery grounds, th en they use selective tidal-stream transport to
reach the shallow productive areas (Rijnsdorp et al., 1985). Plaice
leave their nursery grounds at the end o f their first sum m er th en grad­
ually m ove towards deeper waters w ith increasing size.
T here is a targeted fishery for plaice using b eam traw ls, D anish
seines, a n d gillnets, especially in th e N o rth Sea a n d th e Irish Sea.
T he N o rth Sea stock has increased recently a n d is c u rre n tly fished
at MSY. In th e W estern C hannel, spaw ning-stock biom ass (SSB) is
above BMSY, b u t fishing pressure (F ) is above target. For th e o th er
stocks, th ere is insufficient in fo rm a tio n , a n d p re ca u tio n a ry advice
is given (ICES, 2012).
Ecological value o f coastal habitats
Discussion
T he p re sen t assessm ent dem o n strates clearly the use o f coastal h a b i­
tats b y com m ercially a n d ecologically im p o rta n t species a n d th u s
suggests th e im p o rta n ce o f those habitats to p o p u la tio n dynam ics
a n d fishery yield. O f all ICES-advice species, a large percentage
(44% ) utilizes coastal h abitats d u rin g som e p o rtio n o f th eir life
history, indicatin g the ecological value o f coastal habitats.
M oreover, those advice species using coastal h abitats w ere re sp o n ­
sible for a m ajo rity (71% ) o f the fishery landings in ICES M em ber
C ountries, d e m o n stra tin g the eco n o m ic value o f coastal habitats.
U nfortunately, for m o st species, th ere was in ad e q u ate in fo rm a tio n
to judge th e degree to w hich these coastal h abitats lim it p o p u latio n
g row th a n d fishery p ro d u c tio n . T here is a n obvious lack o f in fo rm a ­
tio n o n ho w fish utilize som e h a b ita t types in th e ICES Area, p a rtic u ­
larly com plex h a rd -b o tto m ha b ita ts such as kelp forests, rocky
shores, a n d m acroalgae, w here m an y census techniques are in a d ­
equate. T he collective in fo rm a tio n suggests th a t these habitats
m ay be essential fo r m a n y species. O ne re co m m e n d a tio n is to
focus fu tu re studies o n these h a b ita t types to a tta in qu an titativ e
d a ta o n fish (b o th p o p u la tio n - a n d individual-level da ta ) a n d
th eir d ependence o n these habitats.
H u m a n p o p u la tio n n u m b ers have b een increasing substantially
in coastal h abitats (A iroldi a n d Beck, 2007). Factors associated w ith
na tu ra l a n d a n th ro p o g e n ic global change, inclu d in g rising tem p e ra ­
tu re a n d sea levels, changes in th e m ag n itu d e o f n u trie n t a n d sedi­
m e n t run -o ff, overfishing, dredging, a n d sand m ining, a n d h a b ita t
loss, presen t increased threats to coastal h ab itats w orldw ide
(K ennesh, 2002; K em p et al., 2005; Lotze et al., 2006). A lthough
m an ag em en t has a tte m p ted to am eliorate adverse effects o f
h a b ita t d egradation, to som e extent, m an y m an ag em en t efforts do
n o t go far e n ough in p ro tec tin g these delicate ha b ita ts a n d the
species th a t rely o n th em . It is estim ated th a t 85% o f E u ro p ea n coast­
lines are degraded (EEA, 1999), a n d public aw areness o f prolonged
ha b ita t losses is lim ited (Lotze, 2004).
In o u r assessm ent, seagrass, shallow in te rtid a l a n d su b tid al soft
b o tto m s, shallow o p e n w ater, m acroalgae, a n d rocky-shore habitats
su p p o rte d all fo u r m ajo r ecological fu n ctio n s— n u rse ry provision,
spaw ning area, m igration, a n d re p ro d u ctiv e areas— am o n g the
species investigated. These habitats are th rea te n e d b y a n th ro p o g e n ic
d istu rb an ce a n d stress d u e to p o llu tio n , e u tro p h ica tio n , and
increased tu rb id ity leading to reduced w ater clarity, im p o rta n t for
seagrass a n d m acroalgae (O rth et al., 2006), as well as direct
h a b ita t d e stru ctio n fro m dredging, sand m ining, a n d destructive
fishing practices, such as traw ling a n d dredging (T u rn er et al.,
1999; Jackson et al., 2001). A synthesis o f the in te rac tio n o f
h u m a n activities w ith m arin e ecosystem s in d icated th a t “n o area
is unaffected b y h u m a n im p a c t” (H a lp ern et al., 2008), a n d o th er
studies show coastal h abitats are th reaten ed b y m ultip le a n th ro p o ­
genic im pacts (Lotze et al., 2006; H a lp ern et al., 2007). V arious
threats m ay affect different coastal h abitats differentially, as p o llu ­
tio n a n d tu rb id ity are im p o rta n t for vegetated habitats (D uarte,
2002), w hile destructive fishing practices are m o st dam ag in g to b io ­
genic habitats, such as oyster reefs a n d m aerl beds (B arbera et al.,
2003). G ear effects from fishery activities have d e trim en tal effects
o n coastal h abitats in m a n y areas (T h ru sh a n d D ayton, 2002;
C huenpagdee et al., 2003; H ix o n a n d Tissot, 2007; H o b d a y et al.,
2011). M oreover, th e c u rre n t d istrib u tio n o f key habitats still
needs to b e quantified, a n d recent efforts to d o so are m ak in g p ro ­
gress in th e rig h t d irec tio n (A gardy a n d Alder, 2005), such as
h a b ita t classifications th ro u g h th e E u ro p ean U n io n N atu re
In fo rm a tio n System (EUNIS) p ro g ram m e (Davies et al., 2004),
a n d th ro u g h m o delling techniques (Bekkby et al., 2008; Sundblad
et al., 2011; G o rm a n et al., 2013). O nly w hen we have qu an titativ e
know ledge o n b o th the spatial d istrib u tio n o f h abitats (e.g. total
area th ro u g h m ap p in g a n d re m o te sensing; q uality th ro u g h p ro d u c ­
tio n per u n it area) a n d o n p o p u la tio n fitness in different h a b ita t
types (i.e. secondary p ro d u c tio n per u n it area in each h a b ita t
type) can w e estim ate th e c o n trib u tio n o f different h a b ita t types
to fish o r invertebrate p ro d u c tio n a n d fisheries.
M a n y o f th e threats to coastal habitats can adversely affect specif­
ic im p o rta n t fish a n d invertebrate species. As o n e exam ple, since
plaice use shallow so ft-b o tto m areas as n u rse ry gro u n d s, th e early
juvenile stage is vulnerable to new c o n stru ctio n a n d in frastru ctu ral
w orks, such as h a rb o u rs a n d ro a d banks, a n d to lan d reclam ation
(R ö n n b äck et al., 2007). A n o th e r th rea t to plaice n u rsery g rounds
is the re d u c tio n in h a b ita t quality a n d q u a n tity caused b y the p ro lif­
e ratio n o f m acroalgae (Pihl etal., 2005), w hich m a y b e a sign o f b o th
e u tro p h ic a tio n a n d a tro p h ic cascade releasing p re d a tio n pressure
o n grazers (Svensson e ta l., 2012).
In a n o th e r species-specific exam ple, since cod d e p en d o n
com plex coastal h abitats d u rin g early dem ersal life stages, loss o f
these h a b ita t types m ay be d e trim en tal to cod p o p u la tio n recovery.
A c o n tin u o u s loss o f large, com plex vegetation d u e to overgrow th b y
filam entous algae caused b y e u tro p h ic a tio n a n d excess se d im e n ta ­
tio n , au g m en ted b y coastal c o n stru ctio n , is a serious th rea t to cod
n u rse ry g ro u n d s (Pihl et al., 2006; A iroldi a n d Beck, 2007).
D eg rad atio n o f these h ab itats m ay also be triggered b y a w eakened
tro p h ic co n tro l, stem m in g fro m decreases in large p re d ato ry fish,
as well as direct losses d u e to harvesting o f algae (T egner and
D ayton, 2000). T hus, overfishing m ay in directly cause d eg rad atio n
o f coastal habitats, w hich m ay give rise to a feedback m ech an ism as
re cru itm e n t o f large p re d ato ry fish is im p a ired (E riksson et al.,
2011). F urther, loss o f biogenic stru ctu res in gravel h abitats d u e to
b o tto m traw ling m ay pose a th rea t to cod n u rse ry h abitats in areas
w ith a n in ten se dem ersal fishery (L indholm etal., 2 004). In a d d itio n
to these, o th e r a n th ro p o g e n ic effects such as o cean acidification and
clim ate w arm in g also likely have negative effects o n fish species, al­
th o u g h th e m ag n itu d e a n d d irec tio n o f such effects d e p en d o n loca­
tio n a n d are difficult to pred ict (Jones, 2014).
Exem plifying th e case o f invertebrates, coastal h ab itats are very
im p o rta n t for b ro w n shrim p, a n d non-selective gear used in
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
T here is little in fo rm a tio n o n the H . gam m arus fishery, a n d a lack
o f official registration o f catches, w hich m ay m ea n th a t p o p u latio n
size is u n d erestim ated . Because o f this, m an ag em en t is difficult, a n d
stock status is n o t well k n o w n (G alparsoro etal., 2009). T otal a n n u al
E u ro p ean landings have varied betw een 1600 a n d 5000 t in the
recent past (H olthuis, 1991; P ro d ö h l et al., 2006), w ith a slow in ­
crease since th e 1970s. M oreover, lobster catches vary considerably
betw een c o u n tries (FAO, 2006; P ro d ö h l eta l., 2006). L obster a q u a ­
c u ltu re is also developing, based o n som e local declines a n d
increases in d e m an d , b u t p ro d u c tio n rates are low. Local p o p u la ­
tio n s sh o u ld be m an ag ed separately as self-recruiting stocks, as
local stocks vary am o n g countries. In som e areas, stocks have
locally collapsed. F or exam ple, the N orw egian stock collapsed
betw een 1960 a n d 1980 (A gnalt e t a l , 2007).
W e have som e detailed in fo rm a tio n o n coastal h a b ita t use for a
few im p o rta n t species, as discussed above. H ow ever, in general,
th ere is p o o r know ledge regarding h a b ita t d ependence even for
m an y c o m m o n species.
659
R. D. Seitz et al.
660
Acknowledgements
W e are in d eb te d to all o u r colleagues in th e ICES w o rk sh o p o n the
“V alue o f C oastal H ab itats for E xploited Species” (held 2 5 - 2 9
June 2012 at ICES h e ad q u arters in C openhagen, D en m ark ) w here
concepts described in this p a p er w ere developed, discussed, a n d
conclusions draw n. W e are also grateful to ICES fo r h osting the
w orkshop, for travel fu n d s for th e p a rticip a tio n o f RL b y US NSF
a n d a U S-N SF W ISE g ran t for fu n d in g the travel o f RS. This is c o n ­
trib u tio n N o. 3310 o f th e V irginia In stitu te o f M arin e Science,
College o f W illiam & M ary.
References
Agardy, T. 2000. Inform ation needs for m arine protected areas: scientif­
ic and societal. Bulletin o f M arine Science, 66: 875-888.
Agardy, T., and Alder, J. 2005. Coastal systems. In Ecosystems and
H um an Well-Being: C urrent State and Trends, Volume 1,
Conditions and Terms, Findings o f the C ondition and Trends
W orking Group o f the M illennium Ecosystem Assessment, pp.
513-549. Ed. by R. Hassan, R. Scholes, and N. Ash. Island Press,
W ashington, DC. 917 pp.
Agnalt, A. L., Kristiansen, T. S., and Jorstad, K. E. 2007. Growth, repro­
ductive cycle, and m ovem ent o f berried E uropean lobsters (Homarus
gammarus) in a local stock off southwestern Norway. ICES Journal o f
M arine Science, 64: 288-297.
Airoldi, L., and Beck, M. W. 2007. Loss, status and trends for coastal
m arine habitats o f Europe. Oceanography and M arine Biology: an
Annual Review, 45: 345-405.
Allain, G., Petitgas, P., Grellier, P., and Lazure, P. 2003. The selection
process from larval to juvenile stages o f anchovy (Engraulis encrasi­
colus) in the Bay o f Biscay investigated by Lagrangian sim ulations
and comparative otolith growth. Fisheries Oceanography, 12:
407-418.
Anibal, J., Esteves, E., Krug, H., and Da Silva, H. M. 1998. Age and
growth in the Alfonsino, Beryx splendens (Berycidae) from the
Azores (central eastern Atlantic). Italian Journal o f Zoology,
65(S1): 215-218.
Armonies, W., and Hellwig-Armonies, M. 1992. Passive settlem ent o f
Macoma balthica spat o n tidal flats o f the W adden Sea and subse­
quent m igration o f juveniles. Netherlands Journal o f Sea Research,
29: 371-378.
Bachelet, G. 1980. Growth and recruitm ent o f the tellinid bivalve
Macoma balthica at the southern lim it o f its geographical distribu­
tion, the Gironde estuary (SW France). M arine Biology, 59:
105-117.
Barbera, C., Bordehore, C., Borg, J. A., Glémarec, M., Graii, J.,
Hall-Spencer, J. M., de la Huz, Ch., et al. 2003. Conservation and
m anagem ent o f N ortheast Atlantic and M editerranean m aerl beds.
Aquatic Conservation: M arine and Freshwater Ecosystems, 13:
65 -7 6 .
Baum ann, H., H inrichsen, H. H., M ollm ann, C., Koster, F. W., Malzahn,
A. M., and Temming, A. 2006. Recruitm ent variation in Baltic Sea
Sprat (Sprattus sprattus) is tightly coupled to tem perature and trans­
po rt patterns affecting the larval and earlyjuvenile stages. Canadian
Journal o f Fisheries and Aquatic Sciences, 63: 2191-2201.
Beck, M. W., Heck, K. L., Jr., Able, K. W., Childers, D. L., Eggleston, D. B.,
Gillanders, B. M., Halpern, B., etal. 2001. The identification, conser­
vation, and m anagem ent o f estuarine and m arine nurseries for fish
and invertebrates. BioScience, 51: 633-641.
Bekkby, T., Rinde, E., Erikstad, L., Bakkestuen, V., Longva, O.,
Christensen, O., Isæus, M., etal. 2008. Spatial probability m odelling
o f eelgrass (Zostera marina) distribution on the west coast o f
Norway. ICES Journal o f M arine Science, 65: 1093-1101.
Bennett, D. B., and Brown, C. G. 1983. Crab (Cancerpagurus) m igra­
tions in the English Channel. Journal o f the M arine Biological
Association o f the UK, 63: 371-398.
Berglund, A. 1982. Coexistence, size overlap and population regulation
in tidal vs. non-tidal Palaem on prawns. Oecologia, 54: 1 -7 .
Bergström, U., Bergström, L., Carien, I., and Isaeus, M. 2011.
GIS-baserade m etoder för a tt kartlägga fiskars livsmiljöer i grunda
havsom ráden. Swedish Environm ental Protection Agency Report,
6427. 74 pp. ISBN 978-91-620-6427-3.
Beukema, J. J., and de Vlas, J. 1989. T idal-current transport o f threaddrifting postlarval juveniles o f the bivalve Macoma balthica from
the W adden Sea to the N orth Sea. M arine Ecology Progress Series,
52: 193-200.
Beverton, R. J. H. 1995. Spatial lim itation o f population size; the concen­
tration hypothesis. N etherlands Journal o f Sea Research, 34: 1-6 .
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
shallow h abitats can destroy these fragile areas. T herefore, th e m ajo r
ecological threats to C. crangon are th o u g h t to involve h a b ita t deg­
ra d a tio n (B ro ad h u rst et al., 2006; ICES, 2011). Towed o r dragged
c o m m ercial fishing gear (b en th ic traw ls o r dredges) are responsible
for over 50% o f to ta l fishery landings (Kelleher, 2005), a n d the
h a b ita t d e stru ctio n a n d bycatch loss b y such gear is substantial
a n d a larm ing (B ro ad h u rst e ta l., 2006).
T he threats to nearshore coastal a n d estuarine ecosystem s to d ay
arise from a vast range o f h u m a n activities, inclu d in g coastal devel­
o p m en t, in d u stria l fishing, aquaculture, u p stre am d am s, a n d w ater
diversions. T he im pacts are m anifold, in clu d in g h a b ita t loss a n d
d egradation, p o llu tio n , e u tro p h ica tio n , h a rm fu l algal bloom s,
changes in freshw ater inflow s o r tidal p atterns, loss o f fish a n d shell­
fish p o p u latio n s, diseases, a n d invasive species. All these can have
im pacts o n n a tu ra l p o p u latio n s a n d also u p o n coastal shellfish
a q u acu ltu re o perations.
It is clear fro m o u r analysis th a t m an y c om m ercially im p o rta n t
species in the ICES A rea utilize coastal habitats. For m o st species,
however, there is insufficient in fo rm a tio n to judge w h eth er these
coastal habitats (o r n o n -c o asta l h ab itats used d u rin g o th er p arts
o f th e life cycle) are actually essential a n d lim itin g to p o p u la tio n
g row th a n d fishery p ro d u c tio n .
Since m an y species use coastal h abitats as spaw ning, feeding, a n d
n u rse ry areas, a n d these life stages usually have very specific h ab itat
dem ands, h a b ita t availability m ay be a b o ttlen eck for m a n y p o p u la ­
tions (Fodrie a n d Levin, 2008; S undblad etal., 2014). F u rth e r studies
are n eeded to a tta in q u a n titativ e d a ta o n coastal h a b ita t use b y fish
a n d invertebrates to aid th e d efin itio n o f key ha b ita ts for p ro tec tio n
a n d re sto ratio n efforts a n d to integrate h a b ita t quality in stock as­
sessm ent a n d ecosystem -based fishery m anagem ent.
P otential consequences o f fu rth e r d eg rad a tio n o f coastal habitats
co u ld include decreased fishery landings, since such a large p e rce n t­
age o f im p o rta n t fishery species depends o n those habitats. G iven
the likelihood for stro n g d ependence u p o n specific coastal habitats
d u rin g juvenile stages in m arin e fish (Juanes, 2007), fu rth e r reviews
q uantifying detailed use o f habitats b y exploited species are a n tic i­
p ated to give a d d itio n al w eight to a rg u m en ts for h a b ita t preserva­
tio n th ro u g h MPAs a n d o th e r m eans (Agardy, 2000). T here have
been efforts a n d policies d irected tow ards coastal a n d m arin e h a b i­
tats o f E urope th a t are th rea te n e d (A iroldi a n d Beck, 2007) a n d
efforts to develop efficient netw orks o f MPAs to p ro tec t such ecosys­
tem s (Sala e ta l., 2002; Fenberg e ta l., 2012). H ow ever, MPAs alone
can n o t p ro tec t h abitats fro m all a n th ro p o g e n ic threats, such as p o l­
lu tio n (A iroldi a n d Beck, 2007), aquaculture, a n d cross-ecosystem
effects o f fishing (E riksson etal., 2011). F u tu re fishery m an ag em en t
efforts need to b e directed n o t o nly at m ain tain in g fish stocks, b u t
also a t preserving a n d resto rin g the h abitats th a t are essential for
fish a n d invertebrate p o p u latio n s, w hich is a m ajo r th ru st o f
ecosystem -based m anagem ent.
Ecological value o f coastal habitats
661
Blanchard, F., and Vanderm eirsch, F. 2005. W arm ing and exponential
abundance increase o f the subtropical fish Capros aper in the Bay
o f Biscay ( 1973-2002). Com ptes Rendus Biologies, 328: 505-509.
Costanza, R., d ’Arge, R., de Groot, R., Färber, S., Grasso, M., H annon, B.,
Limburg, K., et al. 1997. The value o f the w orld’s ecosystem services
and natural capital. N ature, 387: 253-260.
Bolle, L. J., Dapper, R., W itte, J. I., and Van Der Veer, H. W. 1994.
N ursery grounds o f dab (Limanda limanda L.) in the southern
N orth Sea. N etherlands Journal o f Sea Research, 32: 299-307.
Cranford, P., Kam erm ans, P., Krause, C., Mazurié, J., Buck, B., Dolmer,
P., Fraser, D., etal. 2012. An ecosystem-based approach and m anage­
m ent fram ework for the integrated evaluation o f bivalve aquaculture
impacts. A quaculture Environm ent Interaction, 2: 193-213.
Borja, A., Rodríguez, J., Black, K., Bodoy, A., Emblow, C., Fernandes,
T. F., Forte, J., et al. 2009. Assessing the suitability o f a range o f
benthic indices in the evaluation o f environm ental im pact o f fin
and shellfish aquaculture located in sites across Europe.
Aquaculture, 293: 231-240.
Bostock, J., McAndrew, B., Richards, R., Jauncey, K., Telfer, T.,
Lorenzen, K., Little, D., et al. 2010. Aquaculture: global status and
trends. Philosophical Transactions o f the Royal Society o f London,
Series B: Biological Sciences, 365: 2897-2912.
Brown, C. C., and Bennett, D. B. 1980. Population and catch structure o f
the edible crab ( Cancer pagurus) in the English Channel. Journal du
Conseil International p o u r l’Exploration de la Mer, 39: 88-100.
Bryant, D., Rodenburg, E., Cox, T., and Nielsen, D. 1995. ‘Coastlines at
Risk: an Index o f Potential D evelopment-Related Threats to Coastal
Ecosystems,’ W RI Indicator Brief. W orld Resources Institute,
W ashington, DC.
Bunting, S. W. 2013. Principles o f Sustainable Aquaculture: Prom oting
Social, Econom ic and Environm ental Resilience. Routledge,
New York. 320 pp.
Buschbaum, C., D ittm ann, S. R., Hong, J-S., Hwang, I-S., Strasser, M.,
Thiel, M., Valdivia, N., et al. 2009. Mytilid mussels: global habitat
engineers in coastal sediments. Helgoland M arine Research, 63:
4 7 -5 8 .
Cabral, H. N. 2000. Com parative feeding ecology o f sym patric Solea
solea and S. senegalensis, w ithin the nursery areas o f the Tagus
estuary, Portugal. Journal o f Fish Biology, 57: 1550-1562.
Cardinale, M., D örner, H., Abella, A., Andersen, J. L., Casey, J., Döring,
R., Kirkegaard, E., etal. 2013. Rebuilding EU fish stocks and fisheries,
a process u nder way? M arine Policy, 39: 4 3 -5 2 .
Cattrijsse, A., Dankwa, H. R., and Mees, J. 1997. N ursery function o f an
estuarine tidal m arsh for the brow n shrim p Crangon crangon.
Journal ofSea Research, 38: 109-121.
Cattrijsse, A., and Ham pel, H. 2006. European intertidal marshes: a
review o f their habitat functioning and value for aquatic organisms.
M arine Ecology Progress Series, 324: 293-307.
Chanet, B. 2003. Interrelationships o f scophthalm id fishes
(Pleuronectiformes: Scophthalm idae). Cybium, 27: 275-286.
Charm antier, C., H aond, C., Lignot, J-H., and Charm antier-D aures, M.
2001. Ecophysiological adaptation to salinity throughout a life cycle:
a review in hom arid lobsters. Journal o f Experim ental Biology, 204:
967-977.
Chícharo, A., Chícharo, L., Valdés, L., López-Jamar, E., and Ré, P. 1998.
Does the nutritional condition lim it survival potential o f sardine
Sardina pilchardus (W albaum, 1972) larvae off the no rth coast o f
Spain? R N A /D N A ratios and their variability. Fisheries Research,
39: 43 -5 4 .
Chuenpagdee, R., Morgan, L. E., Maxwell, S. M., Norse, E. A., and Pauly,
D. 2003. Shifting gears: assessing collateral im pacts o f fishing
m ethods in US waters. Frontiers in Ecology and the Environm ent,
1: 517-524.
Com m ito, J. A., Como, S., Grupe, B. M., and Dowa, W. E. 2008. Species
diversity in the soft-bottom intertidal zone: biogenic structure, sedi­
m ent, and m acrofauna across mussel bed spatial scales. Journal o f
Experim ental M arine Biology and Ecology, 366: 70-81.
Davies, C. E., Moss, D., and Hill, M. O. 2004. EUNIS H abitat
Classification Revised 2004. Report to EEA and E uropean Topic
Centre on N ature Protection and Biodiversity. O ctober 2004. http:/ /
eunis.eea. e u ro p a .e u /u p lo a d /E U N IS _ 2 0 0 4 _ re p o rt. p d f
(last
accessed 1 Novem ber 2012).
Dorel, D., Koutsikopoulos, C., Desaunay, Y., and M archand, J. 1991.
Seasonal distribution o f young sole (Solea solea (L.)) in the
nursery ground o f the Bay o f Vilaine (N orthern Bay o f Biscay).
N etherlands Journal o f Sea Research, 27: 297-306.
Drake, P., Borlán, A., González-Ortegón, E., Baldó, F., Vilas, C., and
Fernández-Delgado, C. 2007. Spatio-tem poral distribution o f early
life stages o f the E uropean anchovy Engraulis encrasicolus L. w ithin
a E uropean tem perate estuary w ith regulated freshwater inflow:
effects o f environm ental variables. Journal o f Fish Biology, 70:
1689-1709.
D uarte, C. M. 2002. The future o f seagrass meadows. Environm ental
Conservation, 29: 192-206.
EEA. 1999. Coastal and m arine zones. C hapter 3.14. E nvironm ent in the
E uropean U nion at the T urn o f the Century. State o f Environm ent
Report, 1/1999. EEA, Copenhagen, http://w w w .eea.europa.eu/
publications/92-9157-202-0/page314.htm l
(last accessed
1
N ovem ber 2012).
Elliott, M., and Dewailly, F. 1995. The structure and com ponents of
E uropean estuarine fish assemblages. Netherlands Journal of
Aquatic Ecology, 29: 397-417.
Elliott, M., O ’Reilly, M. C., and Taylor, C. J. L. 1990. The forth estuary: a
nursery and overwintering area for N orth Sea fishes. Hydrobiologia,
195: 89-103.
Eltink, A. T. G. W. 1987. Changes in age-size distribution and sex ratio
during spawning and m igration ofW estern mackerel ( Scomber scom­
brus L.). Journal d u Conseil International p o u r l’Exploration de la
Mer, 44: 10-22.
Eriksson, B. K., Sieben, K., Eklöf, J., Ljunggren, L., Olsson, J., Casini, M.,
and Bergström, U. 2011. Effects o f altered offshore food webs on
coastal ecosystems emphasize the need for cross-ecosystem m anage­
m ent. AMBIO: a Journal o fth e H um an Environm ent, 40: 786-797.
FAO (Food and Agriculture O rganization o f the U nited Nations). 1990.
Yearbook o f Fishery Statistics: Catches and Landings, 70. FAO,
Rome. 646 pp.
FAO (Food and Agriculture O rganization o f the U nited Nations). 1999.
The FAO Yearbook o f Fishery Statistics: A quaculture Production,
88/2. FAO, Rome. 178 pp.
FAO (Food and Agriculture O rganization o f the U nited Nations). 2006.
FishStat. http://w w w .fao.org/fi/statist/FISO FT /FISH PL U S.asp.
FAO (Food and Agriculture O rganization o f the U nited Nations). 2012.
Species fact sheets. Homarus gammarus (Linnaeus, 1758). h ttp ://
w w w .fao.org/fishery/species /2 6 4 8 / en.
Fenberg, P. B., Caselle, J. E., Claudet, J., Clemence, M., Gaines, S. D.,
Garcia-Charton, J. A., Gonçalves, E. J., et al. 2012. The science of
E uropean m arine reserves: status, efficacy, and future needs.
M arine Policy, 36: 1012-1021.
Florin, A. B., Sundblad, C., and Bergström, U. 2009. Characterisation of
juvenile flatfish habitats in the Baltic Sea. Estuarine, Coastal and Shelf
Science, 82: 294-300.
Fodrie, F. J., and Levin, L. A. 2008. Linking juvenile habitat utilization to
population dynamics o f California halibut. Limnology and
Oceanography, 53: 799-812.
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Boyden, C. R., and Russell, P. J. C. 1972. The distribution and habitat
range o f the brackish water cockle (Cardium (Cerastoderma)
glaucum) in the British Isles. Journal o f Animal Ecology, 41:
719-734.
Broadhurst, M. K., Suuronen, P., and Hulm e, A. 2006. Estim ating collat­
eral m ortality from towed fishing gear. Fish and Fisheries, 7:
180-218.
Dame, R. F. 1996. Ecology o f M arine Bivalves: an Ecosystem Approach.
CRC Press, Boca Raton, FL. 272 pp.
662
R. D. Seitz et al.
Forrest, B. M., Keely, N. B., Hopkins, G. A., Zebb, S. C., and Clement,
D. M. 2009. Bivalve aquaculture in estuaries: review and synthesis
o f oyster cultivation effects. Aquaculture, 298: 1-15.
H iddink, J. G. 2002. The adaptive value o f m igrations for the bivalve
Macoma balthica. PhD thesis, Rijksuniversiteit Groningen,
Groningen. 172 pp. ISBN 90-9016102-3.
Froese, R., and Pauly, D. 2013. FishBase, W orld W ide Web electronic
publication. Ed. by R. Froese, and D. Pauly, www.fishbase.org,
version (02/2013).
Hilgerloh, G. 1997. Predation by birds on blue mussel M ytilus edulis
beds o f the tidal flats o f Spiekeroog (southern N orth Sea). M arine
Ecology Progress Series, 146: 61-72.
H im m elm an, J. H., and Hamel, J. R. 1993. Diet, behaviour and repro­
duction o f the whelk Buccinum undatum in the northern G ulf o f
St. Lawrence, eastern Canada. M arine Biology, 116: 423-430.
Galparsoro, I., Borja, A., Bald, J., Liria, P., and Chust, G. 2009. Predicting
suitable habitat for the European lobster (Homarus gammarus), on
the Basque continental shelf (Bay o f Biscay), using ecological-niche
factor analysis. Ecological Modelling, 220: 556-567.
Gibson, R. N. 1973. The intertidal m ovem ents and distribu- tion o f
young fish o n a sandy beach w ith special reference to the plaice
(Pleuronectes platessa L.). Journal o f Experimental M arine Biology
and Ecology, 12: 79-102.
Godo, O. R., and Haug, T. 1989. A review ofth e natural history, fisheries,
and m anagem ent o f Greenland halibut (Reinhardtius hippoglos­
soides) in the eastern Norwegian and Barents Seas. Journal du
Conseil International p o u r l’Exploration de la Mer, 46: 6 2 -7 5 .
G orm an, D., Bajjouk, T., Populus, J., Vasquez, M., and Ehrhold, A. 2013.
M odeling kelp forest distribution and biom ass along rocky coast­
lines. M arine Biology, 160: 309-325.
Gorokhova, 1., Fagerberg, T., and Hansson, S. 2004. Predation by herring
( Clupea harengus) and sprat ( Sprattus sprattus) on Cercopagis pengoi
in a western Baltic Sea bay. ICES Journal o f M arine Science, 61:
959-965.
Grioche, A., Harlay, X., Koubbi, P., and Fraga Lago, L. 2000. Vertical
m igrations o f fish larvae: Eulerian and Lagrangian observations in
the Eastern English Channel. Journal o f Plankton Research, 22:
1813-1828.
Guerao, C., and Ribera, C. 1996. Locom otor activity patterns and
feeding habits in the prawn Palaemon serratus (Pennant, 1777)
(Decapoda, Palaem onidae) in the Alfacs Bay, Ebro Delta, Spain.
Crustaceana, 69: 101-112.
Guerao, G., and Ribera, C. 2000. Population characteristics o f the prawn
Palaemon serratus (Decapoda, Palaem onidae) in a shallow
M editerranean Bay. Crustaceana, 73: 459-468.
Haii, S. J., Robertson, M. R., Basford, D. J., and Fryer, R. 1993.
Pit-digging by the crab Cancer pagurus: a test for long-term ,
large-scale effects on infaunal com m unity structure. Journal o f
Animal Ecology, 62: 59-66.
Halpern, B. S., Selkoe, K. A., Micheli, F., and Kappel, C. V. 2007.
Evaluating and ranking the vulnerability o f global m arine ecosystems
to anthropogenic threats. Conservation Biology, 21: 1301-1315.
Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F.,
D ’Agrosa, C., Bruno, J. F., et al. 2008. A global m ap o f hum an
im pact on m arine ecosystems. Science, 319: 948-952.
H art, D. R. 2006. Effects o f sea stars and crabs on sea scallop Placopecten
magellanicus recruitm ent in the M id-Atlantic Bight ( USA). M arine
Ecology Progress Series, 306: 209-221.
H enderson, A., Gamito, S., Karakassis, I., Pederson, P., and Smaal, A.
2001. Use o f hydrodynam ic and benthic models for m anaging envir­
onm ental impacts o f m arine aquaculture. Journal o f Applied
Ichthyology, 17: 163-172.
Henderson,P. A., and Holmes, R. H .A . 1987. O n the population biology
o f the com m on shrim p Crangon crangon (L. ) ( Crustacea: Caridea) in
the Severn Estuary and Bristol Channel. Journal o f the M arine
Biological Association, 67: 825-847.
Hobday, A. J., Sm ith, A. D. M., Stobutzki, I. C., Bulman, C., Daley, R.,
Dam bacher, J. M., Deng, R. A., etal. 2011. Ecological risk assessment
for the effects o f fishing. Fisheries Research, 108: 372-384.
Holland, G. J., Greenstreet, S. P., Gibb, I. M., Fraser, H. M., and
Robertson, M. R. 2005. Identifying sandeel Ammodytes marinus
sedim ent habitat preferences in the m arine environm ent. M arine
Ecology Progress Series, 303: 269-282.
Hollowed, A. B., Aydin, K. Y., Essington, T. E., Ianelli, J. N., Megrey,
B. A., Punt, A. E., and Sm ith, A. D. M. 2011. Experience w ith q uan­
titative ecosystem assessment tools in the northeast Pacific. Fish and
Fisheries, 12: 189-208.
H olthuis, L. B. 1991. FAO species catalogue. Volume 13. M arine lobsters
o f the world. An annotated and illustrated catalogue o f species o f
interest to fisheries know n to date. FAO Fisheries Synopsis. 13
( 125). FAO, Rome. 292 pp.
Howard, A. E. 1980. Substrate controls on the size com position o f
lobster (Homarus gammarus) populations. Journal d u Conseil
International p our l’Exploration de la Mer, 39: 130-133.
Howard, A. E., and Bennett, D. B. 1979. The substrate preference and
burrow ing behaviour o f juvenile lobsters (Homarus gammarus
(L.). Journal o f Natural History, 13: 433-438.
ICES. 2008. ICES Science Plan (2009-1013). International Council for
the Exploration o f the Sea, 8 Septem ber 2008. 14 pp.
ICES. 2010. Report o f the W orking G roup o n M arine H abitat M apping
(W GM H M ), 3 - 7 May 2010, Calvi, Corsica, France. ICES D ocum ent
CM 2010/SSGSUE: 01. 86 pp.
ICES. 2011. R eport o f the W orking G roup o n Crangon Fisheries and Life
H istory (WGCRAN), 1 7 -1 9 May 2011, IJm uiden, The Netherlands.
ICES D ocum ent CM 2011/SSGEF: 11. 38 pp.
ICES. 2012. General context o f ICES advice, http://w w w .ices.dk/
comm unity/advisory-process/Pages/Latest-advice.aspx.
Iglesias, J., Ojea, C., Otero, J. J., Fuentes, L., and Ellis, T. 2003.
C om parison o f m ortality o f wild and released reared 0-group
turbot, Scophthalmus maximus, on an exposed beach (Ría de Vigo,
NW Spain) and a study o f the population dynamics and ecology o f
the natural population. Fisheries M anagem ent and Ecology, 10:
51-59.
Innes, J., and Pascoe, S. 2007. Im pact o n the profitability o f the com m er­
cial UK Crangon fishery. CEMARE Research Paper, 162.
Jackson, J. B., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford,
L. W., Bourque, B. J., Bradbury, R. H., etal. 2001. Historical overfish­
ing and the recent collapse o f coastal ecosystems. Science, 293:
629-637.
Jamieson, A., and Sm ith, P. J. 1987. Atlantic mackerel ( Scomber scombrus
L. ) stocks and genes: a review. Journal du Conseil International pour
l’Exploration de la Mer, 44: 6 6 -7 2 .
Jennings, S., and Pawson, M. C. 1992. The origin and recruitm ent o f
bass, Dicentrarchus labrax, larvae to nursery areas. Journal o f the
M arine Biological Association o f the UK, 72: 199-212.
Jensen, A. C., Collins, K. J., Free, E. K., and Bannister, R. C. A. 1994.
Lobster (Homarus gammarus) m ovem ent o n an artificial reef: the
potential use o f artificial reefs for stock enhancem ent. Proceedings
o f the Fourth International W orkshop o n Lobster Biology and
M anagem ent, 1993. Crustaceana, 67: 198-211.
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Gibson, R. N. 1994. Im pact o f habitat quality and quantity on the re­
cruitm ent o f juvenile flatfishes. Netherlands Journal o f Sea
Research, 32: 191-206.
Gibson, R. N. 1999. The ecology o f the early life stages o f the plaice,
Pleuronectes platessa L.: a review. Bulletin-Tohoku National
Fisheries Research, 62: 17-50.
Gibson, R. N., Robb, L., W ennhage, H., and Burrows, M. T. 2002.
Ontogenetic changes in depth distribution o f juvenile flatfishes in re­
lation to predation risk and tem perature on a shallow-water nursery
ground. M arine Ecology Progress Series, 229: 233-244.
H ixon, M. A., and Tissot, B. N. 2007. C om parison o f trawled vs
untraw led m ud seafloor assemblages o f fishes and m acroinverte­
brates at Coquille Bank, Oregon. Journal o f Experimental M arine
Biology and Ecology, 344: 23 -3 4 .
Ecological value o f coastal habitats
Jensen, O. P., Hansson, S., Didrikas, T., Stockwell, J. D., H rabik, T. R.,
Axenrot, T., and Kitchell, J. F. 2011. Foraging, bioenergetic and p re­
dation constraints o n diel vertical m igration: field observations and
m odelling o f reverse m igration by young-of-the-year herring Clupea
harengus. Journal o f Fish Biology, 78: 449-465.
Jones, C. M. 2014. Can we predict the future: juvenile finfish and their
seagrass nurseries in Chesapeake Bay. ICES Journal o f M arine
Science, 71: 675-682.
Juanes, F. 2007. Role o f habitat in m ediating m ortality during the p ost­
settlem ent transition phase o f tem perate m arine fishes. Journal o f
Fish Biology, 70: 661-677.
Kaiser, M. J., Laing, I., Utting, S. D., and Burnell, G. M. 1998.
Environm ental im pacts o f bivalve m ariculture. Journal o f Shellfish
Research, 17: 59-66.
663
Lotze, H. K. 2004. Repetitive history o f resource depletion and m ism an­
agement: the need for a shift in perspective. M arine Ecology Progress
Series, 274: 269-303.
Lotze, H. K., Lenihan, H. S., Bourque, B. J., Bradbury, R. H., Cooke,
R. G., Kay, M. C., Kidwell, S. M., etal. 2006. Depletion, degradation,
and recovery potential o f estuaries and coastal seas. Science, 312:
1806-1809.
M acDonald, B. A., and T hom pson, R. J. 1985. Influence o f tem perature
and food availability o n the ecological energetics o f the giant scallop
Placopecten magellanicus. I. Growth rates o f shell and som atic tissue.
M arine Ecology Progress Series, 25: 279-294.
M agnússon, J. V. 1996. Greater silver smelt, Argentina silus in Icelandic
waters. Journal o f Fish Biology, 49: 259-275.
M artin, B. T., Zim m er, E. I., Grim m, V., and Jager, T. 2011. Dynamic
energy budget theory m eets individual-based modelling: a generic
and accessible im plem entation. M ethods in Ecology and
Evolution, 3: 445-449.
Kemp, W. M., Boynton, W. R., Adolf, J. E., Boesch, D. F., Bolcourt, W. C.,
Brush, C., Cornwell, J. C., etal. 2005. E utrophication o f Chesapeake
Bay: historical trends and ecological interactions. M arine Ecology
Progress Series, 303: 1-29.
M athieson, S., Cattrijsse, A., Costa, M. J., Drake, P., Elliott, M., Gardner,
J., and M archand, J. 2000. Fish assemblages o f European tidal
marshes: a com parison based on species, families and functional
guilds. M arine Ecology Progress Series, 204: 225-242.
Kennesh, M. J. 2002. Environm ental threats and environm ental future
o f estuaries. Environm ental Conservation, 29: 78-107.
M cClanahan, T. R., Graham , N. A. J., MacNeil, M. A., M uthiga, N. A.,
Cinner, J. E., Bruggemann, J. H., and W ilson, S. K. 2011. Critical
thresholds and tangible targets for ecosystem-based m anagem ent
o f coral reef fishes. Proceedings o f the National Academy of
Sciences o fth e USA, 108: 17230-17233.
Kostecki, C., Rochette, S., Girardin, R., Blanchard, M., Desroy, N., and
Le Pape, 0.2011. Reduction o f flatfish habitat as a consequence o f the
proliferation o f an invasive mollusc. Estuarine, Coastal and Shelf
Science, 92: 154-160.
Kottelat, M., and Freyhof, J. 2007. H andbook o f E uropean Freshwater
Fishes. Publications Kottelat, Cornol, Switzerland. 646 pp.
Koutsikopoulos, C., Fortier, L., and Gagne, J. A. 1991. Cross-shelf dis­
persion o f Dover sole (Solea solea) eggs and larvae in Biscay Bay
and recruitm ent to inshore nurseries. Journal o f Plankton
Research, 13: 923-945.
Kuipers, B. R., and Dapper, R. 1984. N ursery function o f W adden Sea
tidal flats for the brow n shrim p Crangon crangon. M arine Ecology
Progress Series, 17: 171-181.
Laffaille, P., Feunteun, E., and Lefeuvre, J-C. 2000. C om position offish
com m unities in a E uropean m acrotidal salt m arsh (the M ont
Saint-M ichel Bay, France). Estuarine Coastal and Shelf Science, 51:
429-438.
Laffaille, P., Thieulle, L., Feunteun, E., and Lefeuvre, J. 2001.
Com position du peuplem ent piscicole d ’u n petit estuaire anthroprisé ( Le Couesnon, France). Bulletin Français de la Pêche et de la
Pisciculture, 357-360: 191-208.
Launey, S., Ledu, C., Boudry, P., Bonhom m e, F., and Naciri-Graven, Y.
2002. Géographie structure in the European flat oyster ( Ostrea edulis
L. ) as revealed by microsatellite polym orphism . Journal o f Heredity,
93:331-351.
Lindholm , J., Auster, P., and Valentine, P. 2004. Role o f a large m arine
protected area for conserving landscape attributes o f sand habitats
on Georges Bank (NW Atlantic). M arine Ecology Progress Series,
269: 61-68.
Link, J. S., Bundy, A., Overholtz, W. J., Shackell, N., M anderson, J.,
Duplisea, D., Hare, J., et al. 2011. Ecosystem-based fisheries m anage­
m ent in the Northwest Atlantic. Fish and Fisheries, 12: 152-170.
Lintas, C., and Seed, R. 1994. Spatial variation in the fauna associated
w ith Mytilus edulis on a wave-exposed rocky shore. Journal o f
Molluscan Studies, 60: 165-174.
Lipcius, R. N., Eggleston, D. B., Schreiber, S. J., Seitz, R. D., Shen, J.,
Sisson, M., Stockhausen, W. T., et al. 2008. Im portance o f m etapo­
pulation connectivity to restocking and restoration o f m arine
species. Reviews in Fisheries Science, 16: 101-110.
Lopez-Lopez, L., Preciado, I., Velasco, F., Olaso, I., and
Gutiérrez-Zabala, J. L. 2011. Resource partitioning am ongst five
coexisting species o f gurnards (Scorpaeniforme: Triglidae) : Role o f
trophic and habitat segregation. Journal o f Sea Research, 66: 58 -6 8 .
McCormick, S. D., H ansen, L. P., Q uinn, T. P., and Saunders, R. L. 1998.
M ovem ent, m igration, and sm olting o f Atlantic salm on (Salmo
salar). Canadian Journal o f Fisheries and Aquatic Sciences, 55(S1):
77-92.
McKindsey, C. W., Archam bault, P., Callier, M. D., and Olivier, F. 2011.
Influence o f suspended and off-bottom mussel culture o n the sea
b ottom and benthic habitats: a review 1. This review is part o f a
virtual sym posium on current topics in aquaculture o f m arine fish
and shellfish. Canadian Journal o f Zoology, 89: 622-646.
M oriarty, C., and Dekker, W. 1997. M anagem ent o f the European eel.
Fisheries Bulletin (Dublin), 15. 110 pp.
M otos, L., Uriarte, A., and Valencia, V. 1996. The spawning environ­
m ent o f the Bay o f Biscay anchovy (Engraulis encrasicolus L.).
Scientia M arina, 60(Suppl 2): 237-255.
Newell, R. I. E. 2004. Ecosystem influences o f natural and cultivated
populations o f suspension-feeding bivalve molluscs: a review.
Journal o f Shellfish Research, 23: 51-61.
Nichols, J. H., and Lawton, P. 1978. The occurrence o fth e larval stages of
the lobster Homarus gammarus, (Linnaeus, 1758) off the northeast
coast o f England in 1976. Journal d u Conseil International pour
l’Exploration de la Mer, 38: 234-243.
Norderhaug, K. M., Christie, H., Fossa, J. H., and Fredriksen, S. 2005.
Fish-m acrofauna interactions in a kelp (Laminaria hyperborea)
forest. Journal o f the M arine Biological Association o f the UK, 85:
1279-1286.
N ottestad, L., Aksland, M., Beltestad, A., Fernö, A., Johannessen, A., and
M isund, O. A. 1996. Schooling dynamics o f Norwegian spring
spawning herring ( Clupea harengus L. ) in a coastal spawning area.
Sarsia, 80: 277-284.
Nunes, J. P., Ferreira, J. G., Gazeau, F., Lencart-Silva, J., Zhang, X. L.,
Zhu, M. Y., and Fang, J. G. 2003. A m odel for sustainable m anage­
m ent o f shellfish polyculture in coastal bays. Aquaculture, 219:
257-277.
0 ie , G., Makridis, P., Reitan, K. I., and Olsen, Y. 1997. Protein and
carbon utilization o f rotifers (Brachionus plicatilis) in first feeding
o f turbot larvae (Scophthalmus maxim us L.). Aquaculture, 153:
103-122.
Olafsson, E. B. 1986. Density dependence in suspension-feeding and
deposit-feeding populations o f the bivalve Macoma balthica: a field
experiment. Journal o f Animal Ecology, 55: 517-526.
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Kelleher, K. 2005. Discards in the w orld’s m arine fisheries. An update.
FAO Fisheries Technical Paper, 470. Food and Agriculture
Organization o f the U nited Nations, Rome, Italy. 131 pp.
664
O rth, R. J., Carruthers, T. J., Dennison, W. C., D uarte, C. M.,
Fourqurean, J. W., Heck, K. L., Jr, et ai. 2006. A global crisis for sea­
grass ecosystems. Bioscience, 56: 987-996.
Packer, D. B., Cargnelli, L. M., Griesbach, S. J.,and Shumway, S. E. 1999.
Essential Fish H abitat source docum ent. Sea scallop, Placopecten
magellanicus, life history and habitat characteristics. US
D epartm ent o f Com merce NOAA Technical M em orandum
NMFS-NE, 134: 1-21.
Pandian, T. J. 1970. Ecophysiological studies on the developing eggs and
em bryos o f the European lobster Homarus gammarus. M arine
Biology, 5: 154-167.
Penton, P., Davoren, C., Andrews, D., and M ontevecchi, W. A. 2012. A
com parison o f egg developm ental and survival rates in capelin
(Mallotus villosus) o n beach and demersal spawning sites in
Newfoundland. Canadian Journal o f Zoology, 90: 248-256.
Pihl, L., M odin, J., and W ennhage, H. 2000. Spatial distribution patterns
o f newly settled plaice (Pleuronectes platessa L.) along the Swedish
Skagerrak archipelago. Journal o f Sea Research, 44: 6 5 -8 0 .
Pihl, L., M odin, J., and W ennhage, H. 2005. Relating plaice (Pleuronectes
platessa) recruitm ent to deteriorating habitat quality: effects o f
macroalgal bloom s in coastal nursery grounds. Canadian Journal
o f Fisheries and Aquatic Sciences, 62: 1184-1193.
Pihl, L., and W ennhage, H. 2002. Structure and diversity o f fish assem­
blages o n rocky and soft bottom shores o n the Swedish west coast.
Journal o f Fish Biology, 61: 148-166.
Pihl, L., W ennhage, H., and Nilsson, S. 1994. Fish assemblage structure
in relation to m acrophytes and filam entous epiphytes in shallow
non-tidal rocky- and softbottom habitats. Environm ental Biology
o f Fishes, 39:271-288.
Rijnsdorp, A. D., Van Stralen, M., and van der Veer, H. W. 1985. Selective
tidal transport o f N orth Sea plaice larvae Pleuronectes platessa in
coastal nursery areas. Transactions o f the Am erican Fisheries
Society, 114: 461-470.
Rogers, S. I., Millner, R. S., and M ead, T. A. 1998. The distribution and
abundance o f young fish o n the east and south coast o f England
(1981 to 1997). M inistry o f Agriculture, Fisheries and Food,
Centre for Environm ent, Fisheries and A quaculture Science.
Science Series Technical R eport No. 108, CEFAS, Lowestoft. 130 pp.
Rönnbäck, P., Kautsky, N., Pihl, L., Troell, M., Söderqvist, T., and
W ennhage, H. 2007. Ecosystem goods and services from Swedish
coastal habitats: identification, valuation, and im plications o f eco­
system shifts. AMBIO: a Journal o f the H um an Environm ent, 36:
534-544.
Roques, S., Sévigny, J. M., and Bernatchez, L. 2002. Genetic structure o f
deep-water redfish, Sebastes mentella, populations across the N orth
Atlantic. M arine Biology, 140: 297-307.
Sala, E., A burto-O ropeza, O., Paredes, G., Parra, I., Barrera, J. C., and
Dayton, P. K. 2002. A general m odel for designing networks o f
m arine reserves. Science, 298: 1991-1993.
Santos, M. N., and M onteiro, C. C. 1997. The Olhao artificial reef system
(south Portugal): fish assemblages and fishing yield. Fisheries
Research, 30: 33-41.
Seed, R., and Brown, R. A. 1978. Growth as a strategy for survival in two
m arine bivalves, Cerastoderma edule and Modiolus modiolus. Journal
o f Animal Ecology, 47: 283-292.
Sequeira, A., Ferreira, J. C., Hawkins, A. J. S., Nobre, A., Lourenço, P.,
Zhang, X. L., Yan, X., et al. 2008. Trade-offs between shellfish aqua­
culture and benthic biodiversity: a m odelling approach for sustain­
able m anagem ent. Aquaculture, 274: 313-328.
Sheehy, M. R. J., and Prior, A. E. 2008. Progress o n an old question for
stock assessment o f the edible crab Cancer pagurus. M arine Ecology
Progress Series, 353: 191-202.
Pikanwski, R. A., Morse, W. W., Berrien, P. L., Johnson, D. L., and
McMillan, D. G. 1999. Essential Fish H abitat Docum ent: Redfish,
Sebastes spp., life history and habitat characteristics. U.S.
D epartm ent o f Commerce NOAA Technical M em orandum ,
NMFS-NE-132.
Shumway, S. E. (Ed.) 2011. Shellfish A quaculture and the Environm ent.
Wiley-Blackwell, Chichester. 424 pp.
Polte, P., and Asmus, H. 2006. Intertidal seagrass beds (Zostera noltii) as
spawning grounds for transient fishes in the W adden Sea. M arine
Ecology Progress Series, 312: 235-243.
Smaal, A. C. 2002. European mussel cultivation along the Atlantic coast:
production status, problem s and perspectives. Hydrobiologia, 484:
89-98.
Polte, P., Schanz, A., and Asmus, H. 2005. Effects o f current exposure on
habitat preference o f mobile 0-group epibenthos for intertidal sea­
grass beds (Zostera noltii) in the n orthern W adden Sea. Estuarine
Coastal and Shelf Science, 62: 627-635.
Smaal, A. C., and Van Stralen, M. 1990. Average annual growth and con­
dition o f mussels as a function o f food source. Hydrobiologia, 195:
179-188.
Prins, T. C., and Smaal, A. C. 1994. The role o f the blue mussel Mytilus
edulis in the cycling o f nutrients in the Oosterschelde estuary (The
Netherlands). Hydrobiologia, 282: 413-429.
Sims, D. W. 2008. Sieving a living: a review o f the biology, ecology and
conservation status o f the plankton-feeding basking shark
Cetorhinus maximus. Advances in M arine Biology, 54: 171-220.
Steller, D. L., and Cáceres-Martínez, C. 2009. Coralline algal rhodoliths
enhance larval settlem ent and early growth o f the Pacific calico
scallop Argopecten ventricosus. M arine Ecology Progress Series,
396: 49-60.
Prodöhl, P. A., Jorstad, K. E., Triantaphyllidis, A., Katsares, V., and
Triantaphyllidis, C. 2006. Genetic effects o f dom estication, culture
and breeding o f fish and shellfish, and their im pacts on wild popula­
tions. European lobster-H om arus gammarus, pp. 91-98.
Evaluation o f genetic im pact o f aquaculture activities on native
populations: a E uropean network. GENIMPACT Final Report ( EU
contract n. RICA-CT-2005-022802). http://genim pact.im r.no.
Sundblad, G., Bergström, U., and Sandström , A. 2011. Ecological coher­
ence o f m arine protected area networks: a spatial assessment using
species distribution models. Journal o f Applied Ecology, 48:
Rajasilta, M., Eklund, J., Kääriä, J., and Ranta-Aho, K. 1989. The depos­
ition and m ortality o f the eggs o f the Baltic herring Clupea harengus
membras L., o n different substrates in the south-west archipelago o f
Finland. Journal o f Fish Biology, 34: 417-427.
Svensson, C. J., Baden, S., Moksnes, P. O., and Aberg, P. 2012. Temporal
mismatches in p redator-herbivore abundance control algal bloom s
in nutrient-enriched seagrass ecosystems. M arine Ecology Progress
Series, 471: 61 -7 1 .
Read, P., and Fernandes, T. 2003. M anagem ent o f environm ental
im pacts o f m arine aquaculture in Europe. Aquaculture, 226:
139-163.
Swan, S. C., Gordon, J. D. M., and Shimmield, T. 2003. Prelim inary
investigations o n the uses o f otolith m icrochem istry for stock dis­
crim ination o f the deep-water black scabbardfish (Aphanopus
carbo) in the N ortheast Atlantic. Journal o f Northwest Atlantic
Fishery Science, 31: 221-231.
Rijnsdorp, A. D., Van Beek, F. A., Flatman, S., Millner, R. M., Riley, J. D.,
Giret, M., and De Clerck, R. 1992. Recruitm ent o f sole stocks, Solea
solea (L.), in the N ortheast Atlantic. N etherlands Journal o f Sea
Research, 29: 173-192.
112 - 120 .
Sundblad, G., Bergström, U., Sandström , A., andEklöv, P. 2014. Nursery
habitat availability lim its adult stock sizes o f predatory coastal fish.
ICES Journal o f M arine Science, 71: 666-674.
Tegner, M. J., and Dayton, P. K. 2000. Ecosystem effects o f fishing in kelp
forest com m unities. ICES Journal o f M arine Science, 57: 579-589.
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Pihl, L., Baden, S., Kautsky, N., Rönnbäck, P., Soderqvist, T., Troell, M.,
and W ennhage, H. 2006. Shift in fish assemblage structure due to loss
o f seagrass Zostera marina habitats in Sweden. Estuarine Coastal and
Shelf Science, 67: 123-132.
R. D. Seitz et al.
Ecological value o f coastal habitats
Thom pson, I., Jones, D. S., and Dreibelbis, D. 1980. Annual internal
growth banding and life history o f the ocean quahog Arctica islandica
(Mollusca: Bivalvia). M arine Biology, 57: 25-34.
Thrush, S. F., and Dayton, P. K. 2002. D isturbance to m arine benthic
habitats by trawling and dredging: im plications for m arine biodiver­
sity. Annual Review o f Ecology and Systematics, 33: 449-473.
Tully, O., and Céidigh, A. O. 1987. The seasonal and diel distribution o f
lobster larvae (Homarus gammarus (Linnaeus)) in the neuston o f
Galway Bay. Journal du Conseil International po u r l’Exploration
de la Mer, 44: 5 -9 .
Turner, S. J., Thrush, S. F.,Hewitt, J. E., Cum mings, V. J.,andFunnell, G.
1999. Fishing impacts and the degradation o r loss o f habitat struc­
ture. Fisheries M anagem ent and Ecology, 6: 401-420.
van der Veer, H. W. 1986. Im m igration, settlement, and densitydependent m ortality o f a larval and early postlarval 0-group plaice
(Pleuronectes platessa) population in the western W adden Sea.
M arine Ecology Progress Series, 29: 223-236.
van der Veer, H. W., Berghahn, R., Miller, J. M., and Rijnsdorp, A. D.
2000. Recruitm ent in flatfish, w ith special emphasis on N orth
Atlantic species: progress m ade by the Flatfish Symposia. ICES
Journal o f M arine Science, 57: 202-215.
Vasconcelos, R. P., Eggleston, D. B., Le Pape, O., and Tulp, I. 2014.
Patterns and processes o f habitat-specific dem ographic variability
in exploited m arine species. ICES Journal o f M arine Science, 71:
664-673.
Verissimo, A., McDowell, J. R., and Graves, J. E. 2011. Population struc­
ture o f a deep-water squaloid shark, the Portuguese dogfish
(Centroscymnus coelolepis). ICES Journal o f M arine Science, 68:
555-563.
Verissimo, A., McDowell, J. R., and Graves, J. E. 2012. Genetic popula­
tion structure and connectivity in a commercially exploited and
wide-ranging deepwater shark, the leafscale guiper (Centrophorus
squamosus). M arine and Freshwater Research, 63: 505-512.
Voss, R., Köster, F. W., and Dickm ann, M. 2003. Com paring the feeding
habits o f co-occurring sprat (Sprattus sprattus) and cod (Gadus
morhua) larvae in the Bornholm Basin, Baltic Sea. Fisheries
Research, 63: 97-111.
Wahle, R., and Steneck, R. 1991. R ecruitm ent habitats and nursery
grounds o f the Am erican lobster Homarus americanus: a dem o­
graphic bottleneck? M arine Ecology Progress Series, 69: 231-243.
Walter, U., and Liebezeit, C. 2003. Efficiency o f blue mussel (Mytilus
edulis) spat collectors in highly dynamic tidal environm ents o f the
Lower Saxonian coast (southern N orth Sea). Biomolecular
Engineering, 20: 407-411.
W orm , B., Barbier, E. B., Beaum ont, N., Duffy, J. E., Folke, C., Halpern,
B. S., Jackson, J. B. C., et al. 2006. Im pacts o f biodiversity loss on
ocean ecosystem services. Science, 314: 787-790.
Ysebaert, T., H art, M., and H erm an, P. M. J. 2009. Im pacts o f bottom
and suspended cultures o f mussels Mytilus spp. o n the surrounding
sedim entary environm ent and m acrobenthic biodiversity.
Helgoland M arine Research, 63: 59-74.
H andling editor: E m ory Anderson
Downloaded from http://icesjms.oxfordjournals.org/ at Lib Netherlands Inst for Sea Res on August 13, 2014
Uzars, D., and Plikshs, M. 2000. Cod ( Gadus morhua L.) cannibalism in
the Central Baltic: interannual variability and influence o f recruit
abundance and distribution. ICES Journal o f M arine Science, 57:
324-329.
665