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Conditional Responses of Benthic Communities to
Interference from an Intertidal Bivalve
Cari Van Colen1*, Simon F. Thrush2'3, Magda Vincx1, Tom Ysebaert4
1 Ghent University, D epartm ent o f Biology, Marine Biology Research Group, Ghent, Belgium, 2 National Institute of W ater and Atmospheric Research, Hamilton, New
Zealand, 3 University of Auckland, School o f Environment, Auckland, New Zealand, 4 Netherlands Institute for Sea Research (NIOZ-Yerseke), Yerseke, The Netherlands
Abstract
H abitat-m odifying organisms tha t im pact o th e r organisms and local fun ctioning are im p ortan t in determ ining ecosystem
resilience. However, it is often unclear how the outcom e o f interactions perform ed by key species varies depending on the
spatial and tem poral disturbance context w hich makes the prediction o f disturbance-driven regime shifts difficult. We
investigated the strength and generality o f effects o f the filte r feeding cockle Cerastoderma edule on its am bient intertidal
benthic physical and biological environm ent. By com paring the m agnitude o f the effect o f experim ental cockle removal
between a non-cohesive and a sheltered cohesive sedim ent in tw o different periods o f the year, we show th a t the outcom e
o f cockle interference effects relates to differences in physical disturbance, and to tem poral changes in suspended sedim ent
load and ontoge ne tic changes in organism traits. Interference effects were only present in the cohesive sediments, tho ugh
the effects varied seasonally. Cockle presence decreased only the density o f surface-dwelling species suggesting that
interference effects were particularly m ediated by bioturb ation o f the surface sediments. Furthermore, density reductions in
the presence o f cockles were m ost pronounced during the season when larvae and juveniles were present, suggesting that
these life history stages are m ost vulnerable to interference com petition. We furthe r illustrate tha t cockles may enhance
benthic microalgal biomass, m ost likely th ro u g h the reduction o f surface-dwelling grazing species, especially in periods w ith
high sedim ent load and supposedly also high b ioturb ation rates. O ur results emphasize th a t the physical disturbance o f the
sedim ent may obliterate biotic interactions, and tha t tem poral changes in environm ental stressors, such as suspended
sediments, may affect the outcom e o f key species interference effects at the local scale. Consequently, natural processes
and anthropogenic activities th a t change bed shear stress and sedim ent dynamics in coastal soft-sedim ent systems w ill
affect cockle-m ediated influences on ecosystem properties and therefore the resilience o f these systems to environm ental
change.
C i t a t i o n : Van Colen C, Thrush SF, Vincx M, Ysebaert T (2013) Conditional Responses of Benthic Communities to Interference from an Intertidal Bivalve. PLoS
ONE 8(6): e65861. doi:10.1371/journal.pone.0065861
E d i t o r : Philippe Archambault, Université du Q uébec à Rimouski, Canada
R e c e i v e d November 22, 2012; A c c e p t e d April 28, 2013; P u b l i s h e d June 18, 2013
C o p y r i g h t : © 2013 Van Colen e t al. This is an open-access article distributed under the terms of th e Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided th e original author and source are credited.
F u n d i n g : CVC is a postdoctoral fellow o f th e Flemish Fund for Scientific Research FWO (FWO-1.2.380.11.N.00). Additional financial support for this study cam e
from th e special research fund o f G hent University through project BOF-GOA 01GA1911W and a Marie Curie International Fellowship to SFT (FP7-PEOPLE-2007-42-IIF-ENV221065). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of th e manuscript.
C o m p e t i n g I n t e r e s t s : The authors have declared th a t no com peting interests exist.
* E-mail: carl.vancolen@ugent.be
coastal soft-sedim ent c o m m u n ity co m p o sitio n , dynam ics, species
b e h a v io r a n d ecosystem fu n c tio n in g [6,7,8], F u rth e rm o re ,
su sp en d ed sedim ents de cre ase th e fitness o f filter feeding
o rganism s d irectly b y d e cre asin g filtra tio n ra te a n d a b so rp tio n
efficiency th a t red u ces n e t en erg y intake [9], a n d ind irectly by
in cre asin g tu rb id ity a n d h en ce d e cre asin g w a te r c o lu m n
p rim a ry p ro d u c tio n , i.e. food reso u rce availability. M o re o v er,
changes in sed im en t dynam ics th a t im p a c t th e c o n d itio n a n d
b e h a v io r o f key species th a t a re involved in m a in ta in in g
ecosystem resilience, such as h a b ita t-m o d ify in g o r ecosystem
en g in e erin g organism s, sensu Jo n e s et al. [10], e.g. [11], h ave the
p o te n tia l to shift the in te rac tio n s w ith in a n ecosystem [12],
th e re b y a lte rin g ecosystem stability. T h is is likely to have farre a c h in g c o n seq u en ces since th e resilience o f ecosystem s
re p re se n ts a n in su ra n ce again st p o ten tially adverse changes in
th e delivery o f ecosystem goods a n d services.
In general, experim ental field studies indicate strong contextdepen d en cy in the strength o f ecosystem engineering effects
m ed iated by e n vironm ental setting. F or exam ple, N orkko et al.
[13] illustrate th a t facilitation strength o f a filter feeding bivalve on
Introduction
C o astal soft-sedim ent h a b ita ts such as estilarm e tidal flats
re p re se n t som e o f o u r m ost v a lu e d ecosystem s a n d are
c h a ra c te riz e d b y a h ig h biom ass o f in v e rte b ra te b e n th ic
o rganism s th a t sustain coastal foodw ebs [1,2]. H o w ev er, these
p ro d u c tiv e system s increasingly e x p erien c e d istu rb an c es w ith
th e e x p a n d in g h u m a n p o p u la tio n a n d e x p lo itatio n o f coastal
area s [3,4], F o r ex am p le, changes in se d im e n tatio n regim es a n d
w a te r-b o rn e su sp en d e d sed im en t c o n ce n tra tio n s (SSCI) are
asso ciated w ith c h an g es in lan d -u se a n d e n g in e erin g activities
in th e co astal zo n e, a n d in cre ased ra te s o f sed im en t lo ad in g
adversely affect coastal soft-sedim ent ecosystem b iodiversity a n d
ecological v alu e [5], S u sp en d e d sedim ents m ay deposit or
re m a in su sp en d ed d e p e n d in g o n th e physical forces associated
w ith w aves a n d c u rre n ts, w h ich m ay v a ry spatially a n d
te m p o rally a n d h e n ce affect th e b a la n c e b e tw ee n d e position
a n d (re)suspension. N evertheless, b o th processes influence
sed im en t c o m m u n ity c o m p o sitio n a n d fun ctio n in g . N u m e ro u s
studies illu strate th a t terrig en o u s sed im en t d ep o sitio n affects
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Context-Dependent Cockle Effects on Benthos
Materials and M ethods
benthic com m unities decreased w ith increased suspended sedi­
m e n t co n ce n tra tio n in th e w a ter colum n, w hile T h ru sh et al. [14]
indicate th a t th e negative effects o f a deposit feeding bivalve on
ju venile bivalves increased w ith h y d rodynam ic stress. In addition,
th e m ag n itu d e o f effects m ay also d e p en d on th e local c om m unity
c om position a n d the strength o f specific species interactions. F or
exam ple, species living in the u p p e r few centim eters o f the
sedim ent are p a rticu la rly affected by sedim ent erosion [15] and
organism s th a t affect sedim ent erodibility m ay therefore p a rtic ­
ularly affect survival a n d d istribution o f juveniles w hich are
un a b le to b u rro w deep, th ere b y com prom ising n a tu ra l d e m o ­
grap h ic p o p u latio n processes. T h e exam ples above highlight the
im p o rta n ce o f in te g ratin g spatio -tem p o ral d ep en d en cy in e x p er­
im e n tal designs to investigate how stressor-m ediated changes in
beh av io r o f hab itat-m o d ify in g organism s affect ecosystem p ro p ­
erties.
T h e filter feeding cockle Cerastoderma edule (M ollusca: Pelecy­
poda) lives b u ried in the top few centim eters o f coastal sedim ents
w here it can o ccur in densities > 1 0 0 0 in d .m 2 [16,17]. Field
observations indicate a shift tow ards a less diverse assem blage
d o m in a ted by deep-living species w h ere C. edule is a b u n d a n t [18].
T h is species m odifies its h a b ita t by alterin g n u trie n t processing,
d epleting the w ater colum n o f food a n d larvae, an d by changing
c om position an d resuspension o f th e sedim ent via vertical and
h o rizo n tal m ovem ents, nam ely shaking an d valve clapping [19—
21]. F u rth e rm o re , m esoscosm experim ents reveal th a t e n h an c ed
suspended sedim ents m ay affect the o utcom e o f cockle in te ra c ­
tions w ithin th e ecosystem because suspended sedim ents stim ulate
shell shaking a n d valve clapping [22] w ith im plications for
biodiversity a n d ecosystem functioning (e.g. in terference co m p e­
tition a n d sedim ent resuspension). C onsequently, C. edule can be
view ed w ithin a n etw ork o f direct a n d in d irect interactions th at
su p p o rt ecosystem functioning an d biodiversity w hich are
m ed ia te d by bio-physical processes th a t define intrinsic ecological
dynam ics.
T h e re is grow ing evidence th a t in teractio n s b etw een the
im p a c t o f stressors a n d key species-m ediated ecological dynam ics
c an initiate th resh o ld responses a n d increase th e risk o f a regim e
shift ([23] a n d references therein). C onseq u en tly , g ain in g insights
in stresso r-m ed iated outcom es o f ecosystem e n g in eerin g in te ra c ­
tions will c o n trib u te to a b e tte r assessm ent o f th e stability o f
fu n c tio n in g in soft-sedim entary h a b ita ts th a t are subject to
e n v iro n m en ta l change, i.e. resilience. T h is study investigated the
stre n g th a n d gen erality o f th e effects o f C. edule on its in te rtid a l
physical a n d biological e n v iro n m en t a n d c o n tra sted these effects
b etw een tw o different e n v iro n m en ta l settings. W e c o m p a re d the
m ag n itu d e o f th e effect o f e x p erim e n tal cockle rem o v al betw een
cohesive a n d non-cohesive sedim ents d u rin g th e re c ru itm e n t an d
p o st-re c ru itm e n t p e rio d o f th e sam e year. C o m p a rin g the
o u tco m e o f cockle in terferen ce b etw een a strongly physically
stressed non-cohesive sedim ent versus a m o re stable cohesive
sedim ent should enable in te rp re ta tio n o f th e im p o rta n c e o f
e n v iro n m en ta l physical forcing a n d differences in co m m u n ity
c o m position in d e te rm in in g cockle effects. Inclusion o f tem p o ral
v ariability in th e study design allows the assessm ent o f effects on
tem p o rally available juveniles, an d the im p o rta n ce o f tem p o ral
c hanges in su spended sedim ent c o n ce n tra tio n s in gov ern in g
cockle in terferen ce effects. W e exp ected th a t cockle effects on
sedim ent physical a n d biological p ro p e rties w ould be m ost
p ro n o u n c e d in perio d s w h en ju v en ile organism s are p re se n t and
su spended sedim ent c o n ce n tra tio n s are highest, th o u g h physical
d istu rb an c e o f the sedim ent b e d resulting from h y d ro d y n am ic
forces m ay overw helm local in terferen ce effects.
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S tudy sites: physical c o n d itio n s and a m b ie n t cockle
p o p u la tio n s
Cockle densities w ere m an ip u lated in 2011 at two study sites,
w hich are characterized by contrasting physical a n d biological
properties (see results a n d below). O n e study site was located in the
m id-intertidal zone o f the Paulinaschor, in the W esterschelde
estuary, w hereas the o th er study site was located in the m idin tertidal zone o f the tidal flat n e a r V iane in the O osterschelde
estuary (Figure SI in File SI). E m ersion tim e at b o th study sites
varied betw een 5 0 -6 0 % , b u t the study site a t V iane w as m ore
exposed to the p re d o m in an t southw estern w inds a n d experienced
h igher tidal cu rre n t velocities (3 0-40 cm.s *) th a n the study site at
P aulinaschor (20-25 cm.s *). S uspended sedim ent concentrations
(SSC) w ere h igher at P aulinaschor (8.56—165 m g.L :), th en at
V iane (2.71—54.1 m g.L :) over the course o f the experim ent. In
general, SSC was ab o u t twice as high in a u tu m n an d w inter th an
in spring an d sum m er at b o th study sites (Figure 1). Sedim ent at
P aulinaschor was cohesive an d consisted p re d o m in an tly o f silt
(m edian grain size = 49.4 J im ), w hereas sedim ent at V iane was
non-cohesive consisting p re d o m in an tly o f fine a n d m edium sand
(m edian g rain size = 184.9 J im ). In addition, the non-cohesive
sedim ent con tain ed less p ore w ater a n d low er organic m a tte r
derived from p rim a ry p ro duction, i.e. chloroplastic photo p ig m en t
equivalents (CPE) (Figure 2). Study sites are fu rth er referred to as
cohesive site (Paulinaschor) an d non-cohesive site (Viane).
T h e adult cockle p o p u latio n in 2011 consisted o f tw o cohorts
(recruited in 2009 an d 2010) at b o th sites. A verage adult density
was 1 6 .9 ± 1 .6 SE in d .0.25 m 2 at the non-cohesive site and
18 . 0 ± 7.5 ind.0.25 m 2 at the cohesive site.
Experim ental design and sam ple processing
F o u r p a ire d 0.5 m x 0 .5 m (i.e. 0.25 m 2) experim ental plots w ere
selected along a 25 m transect w hich was ran d o m ly p laced parallel
to the tide line in the m id in tertidal zone o f b o th study sites.
160 -
3 120 -
40 -
20
-
I---- 1---- 1-----1-----1-T—I
tH
T—I
tH
T—I
rH
TH
rH
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T—I
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Figure 1. Tem poral v ariatio n in suspended sedim ent concen­
tra tio n (SSC) at both study sites in 2 0 1 1. Black b a rs in d ic a te th e
tw o e x p e rim e n ta l p e rio d s . SSC w e re re trie v e d fro m t h e p u b lic url: w w w .
w a te rb a s e .n l. SSC a t P aulina (black lines) w a s c a lc u la te d as th e a v e r a g e
v a lu e fro m re c o rd in g s a t T e rn e u z e n , V lissingen a n d H a n sw e ert, w h e re a s
SSC a t V iane (grey lines) w a s c a lc u la te d a s th e a v e r a g e v a lu e from
re c o rd in g s a t Z ijpe a n d W issenkerke; s e e F ig u re SI in File SI for
in d ic a tio n o f s a m p lin g lo c a tio n s. Solid lines in d ic a te a v e r a g e c o n c e n ­
tra tio n s , d a s h e d lines th e m in im u m a n d m a x im u m c o n c e n tr a tio n
r e c o rd e d a t a s a m p lin g lo c a tio n .
d o i:1 0.13 7 1 /jo u rn a l.p o n e .0 0 6 5 8 6 1 .g001
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Context-Dependent Cockle Effects on Benthos
200
I
o
o
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ad d ed cockles was 2 8 .6 ± 0 .1 SE m m for the trial du rin g
recruitm ent, a n d 2 9 .4 ± 0 .1 SE m m for the po st-recru itm en t trial.
T w o days after rem oval o f the fram es, we collected sam ples in
the o u ter rim o f each N C p lo t a n d from the ad jacen t am b ien t
un m an ip u lated sedim ent to assess poten tial artifacts o n sedim ent
physical a n d biological properties associated w ith d eploym ent o f
the fram es a n d nets. D eploym ent o f fram es did n o t significantly
influenced sedim ent particle size, w ater content, redox potential
discontinuity layer depth, a n d m acro fau n a c om m unity com posi­
tion (except ad u lt cockles) du rin g b o th study periods a t b o th sites,
tho u g h C P E was slightly low er in the plots as c o m p a red to the
am b ie n t sedim ent a t the start o f the po st-recru itm en t trial, i.e.
respectively —6.9 pg.g 1 a n d —1.9 pg.g 1 a t the cohesive a n d the
non-cohesive site (T able S I in File SI).
C ockle effects o n sedim ent physical a n d biological properties,
a n d the n u m b e r o f a d u lt cockles p re sen t in the plots, w ere
d e term in ed after six weeks. T h e n u m b e r o f a d u lt cockles was
assessed by sieving the in n er 30 cm diam eter o f each plot. A dult
cockle densities in the in n er 30 cm d iam eter o f the C plots after six
weeks was, on average, respectively 4.8 a n d 5.0 du rin g the
re cru itm e n t trial a n d the po st-recru itm en t trial in the non-cohesive
sedim ents, a n d respectively 3.8 a n d 4.0 in the cohesive sedim ents
d u rin g the re cru itm e n t a n d po st-recru itm en t trial. C ockle densities
thus e qualed 13-17 individuals p e r C plo t across all treatm ents
a n d trials, w hile only one a d u lt cockle was found in all N C plots.
Cockle effects on b e n th ic com m unities w ere d e term in ed from
th ree 10 cm (i.d.) p erspex corers th a t w ere ran d o m ly collected to a
d e p th o f 10 cm in the in n er 30 cm d iam eter o f each C a n d N C
plot. T hese sam ples w ere pooled a n d fixed o n a neutralized 8%
fo rm aldehyde-tapw ater solution. Subsequently, sam ples w ere
sieved over a 1 m m m esh in the laboratory, a n d the organism
re ta in e d o n the sieve w ere co u n ted a n d identified to the lowest
possible taxonom ic level. Sim ilarly, w e collected th ree 3.2 cm (i.d.)
perspex corers to a d e p th o f 5 cm from the in n er 30 cm o f each
p lo t in o rd e r to quantify sedim ent properties. F rom each corer we
stored the u p p e r 0.5 cm o f sedim ent o n dry ice a n d a t —20°C (for
sedim ent com position a n d w ater content, tw o samples) a n d
—80°C (for C PE concentrations, one sample) u p o n arrival in the
lab o ra to ry aw aiting furth er processing. Sam ples w ere w eighed w et,
lyophilized in the d a rk a n d w eighed again to yield absolute w ater
co n te n t (%). Sedim ent com position was d e term in ed from the dry
sedim ent using M alvern laser diffraction a n d C PE , i.e. sum o f
chlorophyll a a n d its d eg rad a tio n products (phaeopigm ents), was
d e term in ed follow ing Jeffrey et al. [26] using F1PLC o f the
su p e rn ata n t th a t was extracted from the freeze-dried sedim ent by
a d d in g 10 m l 90% acetone.
160
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120
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M ay-June
Oct-Nov
cohesive
M ay-June
2
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Oct-Nov
non-cohesive
Figure 2. S p atio -tem p oral effects o f cockle tre a tm e n t on
physical sedim ent properties. S e d im e n t m e d ia n g ra in size, w a te r
c o n te n t, a n d c h lo ro p la s tic p h o to p ig m e n t e q u iv a le n t (CPE) c o n c e n tr a ­
tio n , s h o w n a s m e a n ± SE fo r p lo ts w ith o u t (NC) a n d w ith (C) c o ck les in
th e tw o c o n tra s tin g s e d im e n ts d u rin g b o th e x p e rim e n ta l trials, i.e.
d u rin g r e c ru itm e n t (M a y -Ju n e ) a n d p o s t-re c ru itm e n t (O c to b e r-N o v e m b er).
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 5 8 6 1 .g 0 0 2
D istances b etw een pairs o f plots was 5 m . Cockle densities w ere
m an ip u lated by incu b atin g each plo t for 10 days u n d e r a nylon
1 m m m esh-sized net, th a t was placed flush w ith th e sedim ent
surface, using m etal fram es. T his technique chased cockles to the
sedim ent surface so th a t they could easily a n d effectively be
rem oved. D u rin g the sam e low tide, 17 a d u lt alive cockles (i.e.
average am b ie n t a d u lt density) th a t w ere collected a t the study site
w ere a d d ed into one ran d o m ly assigned plo t p e r pair, yielding one
plo t w ith cockles (C) a n d one plo t w ith o u t cockles (NC) p e r pair.
Cockles w ere a d d ed using a 0 .5 x 0 .5 m fram e w ith 25 1 0 x 1 0 cm
quadrats, ensuring a hom ogenous distribution o f the study
organism s a t the start o f the experim ent. W e p erfo rm ed the
ex p erim en t in tw o different periods o f the year; i.e. du rin g
re cru itm e n t (M ay-June, fram e deploym ent o n A pril 18th a n d 19th)
a n d po st-recru itm en t (O cto b er-N o v e m b er, fram e deploym ent on
S eptem ber 22nd a n d 23th) a t b o th study sites [24,25]. T h e average
size o f a d d ed cockles was 2 8 .9 ± 0 .1 SE m m a t the non-cohesive
site for the trial du rin g the re cru itm e n t period, a n d 2 8 .0 ± 0 .1 SE
m m for the po st-recru itm en t trial. A t the cohesive site, the size o f
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Data analysis
T w o-w ay Analysis o f Sim ilarities [27] was used to com pare
com m unity com position b etw een study sites a n d experim ental
trials, using the sam ples from the a m b ie n t sedim ent th a t w ere
collected two days after rem oval o f the fram es.
W e c o m p a red the m agnitude o f the effect o f cockle presence (C)
versus experim ental cockle rem oval (NC) in two contrasting
sedim ent types. G iven the general h igher variability in noncohesive sedim ents a n d the difference in d o m in a n t species
presence betw een b o th sedim ent types, we analyzed the effects
o f cockle interference using a tw o-w ay factorial generalized linear
m odel for each sedim ent type separately. T h is m odel included the
fixed factors Cockle (present, rem oved) a n d T im in g (recruitm ent,
po st-recru itm en t period), as tim ing o f the ex p erim en t was
deliberately chosen to rep resen t seasonal changes in SSC a n d
presence o f juveniles w hich m ay affect the outcom e o f cockle
interference o n sedim ent properties. G a m m a e rro r structures,
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Context-Dependent Cockle Effects on Benthos
using a log-link function w ere used for m odels o f total density a n d
species density, w hile n o rm al e rro r structures w ere used for
general c om m unity attributes (species richness, P ielou’s evenness,
a n d S im pson’s index o f diversity) a n d physical sedim ent properties.
D ensities are expressed as individuals p e r 0.024 m 2, i.e. the total
surface o f the th ree pooled corers. W e rem oved typical m eio-,
hyper- a n d epifaunal tax a from the biotic dataset since these
organism s w ere n o t sam pled qualitatively. L oge transform ation
was applied to m eet the assum ption o f w ithin group variance
hom ogeneity (Levene test), if needed. A lternatively, if L oge
tran sfo rm atio n was n o t successful in p ro d u c in g hom ogeneity o f
variance, we cond u cted tw o-w ay factorial p e rm u tatio n al analysis
o f v ariance after d a ta sim ilarities w ere calculated using E uclidean
distances, a n d checked for m ultivariate dispersion [28] .W e
assessed cockle effects o n the density o f the five m ost d o m in a n t
species from each site, w hich com prised 91 a n d 71% o f the total
density a t the cohesive a n d non-cohesive site, respectively. Since
we expected th a t surface-dw elling organism s th a t feed o n the
surface sedim ent a n d th a t have ra th e r lim ited dispersal capacities
d u rin g th eir a d u lt life stage w ould be particularly influenced by
cockles, w e additionally analyzed cockle effects on the diversity
a n d density o f this pool o f organism s separately. T hese surface
deposit feeders th a t have lim ited dispersal capacities as c o m p a red
to the highly m obile am phipods are fu rth er referred to as L D SD F.
the re cru itm e n t trial in M a y -Ju n e (Figure 3). C ockle presence
significantly decreased the density o f A. marioni, P. elegans a n d
juveniles o f M . balthica d u rin g a t least one o f the trials (T able S2 in
File SI). D ensity o f A. marioni was red u ced b y 35% d u rin g the
re cru itm e n t trial, w hile density o f M . balthica recruits was reduced
by 65% d u rin g the po st-recru itm en t trial (Figure 4). T h e density o f
P. elegans was, o n average, red u ced by 45% in M a y -Ju n e a n d by
51% in O c to b e r-N o v e m b e r. N o detectable effects w ere a p p are n t
for O ligochaeta spp. a n d H. filiformis. D iversity a n d evenness o f the
L D S D F c om m unity was lowest in the C plots a t the e n d o f the
po st-recru itm en t trial (Figure 3).
Cockle effects in non-cohesive sedim ents
N o n e o f the m easu red physical a n d biological sedim ent
p roperties was significantly influenced by the cockle trea tm e n t in
the non-cohesive sedim ents (T able S3 in File SI). Flowever, some
sedim ent p roperties revealed significant tem poral variation,
in d ep e n d en t o f cockle presence. Sim ilar to the cohesive sedim ents,
m edian g rain size decreased du rin g the p o st-recru itm en t trial
(Figure 2). In general, the density o f the m ost d o m in a n t species was
low er d u rin g the po st-recru itm en t trial in O c to b er-N o v e m b er,
except for Hydrobia ulvae (Figure 4). T h e latter species was a b sen t in
M a y -Ju n e , b u t was the m ost d o m in a n t m em b e r o f the com m unity
in O c to b e r-N o v e m b e r. H ow ever, these changes in species density
did n o t significantly affected overall a n d L D S D F com m unity
density, diversity a n d evenness.
Results
Species assem blage o f non-cohesive and cohesive
sedim ents
Discussion
B enthic c om m unity com position differed significantly am o n g
study sites a n d over tim e (A N O SIM , site R = 0.995, pCO.OOl;
tim e R = 0.289, p = 0.003). O verall, Polychaeta (4 species), a n d
C ru stacea (3 species) com prised 88% o f the individuals p re sen t at
the non-cohesive study site, while Polychaeta (8 species) a n d
O ligochaeta spp. w ere the m ost d o m in a n t tax a a t the cohesive
study site com prising, respectively, 88 a n d 7% o f the total n u m b er
o f individuals. A t the cohesive site, L D S D F com prised 86% o f the
total com m unity, while only 59% o f the organism s w ere L D S D F
a t the non-cohesive site.
D u rin g b o th trials, a higher total density a n d species richness
w ere p re sen t in the cohesive sedim ents, b u t total com m unity
diversity a n d evenness was h igher in the non-cohesive sedim ents
(Figure 3, a -d ). Sim ilarly, L D S D F species richness a n d total
density w ere h igher in the non-cohesive sedim ents, while L D S D F
evenness was h igher du rin g b o th trials, a n d L D S D F diversity was
h igher d u rin g in M ay^June, in the non-cohesive sedim ents
(Figure 3, e—f). T h e five m ost d o m in a n t species a t the cohesive
site w ere the L D S D F Aphelochaeta marioni, pygospio elegans a n d
juvenile recruits o f Macoma balthica, a n d the subsurface deposit
feeding species Heteromastus filiformis a n d O ligochaeta spp. In
contrast, the L D S D F species Scoloplos armiger a n d Pygospio elegans,
the m obile species Hydrobia ulvae a n d Urothoe poseidonis, a n d the filter
feeding recruits o f C. edule w ere the m ost d o m in a n t species a t the
non-cohesive site.
W e have ex am in ed the generality o f the in teractio n b etw een a
filter feeding infaunal bivalve, C. edule, a n d its a m b ie n t biotic a n d
physical environm ent. By m an ip u latin g cockle densities in two
contrasting sedim ent types (i.e. a sheltered cohesive tidal flat vs. a
physically stressed non-cohesive tidal flat) in two different periods
(i.e. du rin g re cru itm e n t a n d p o st-recru itm en t phase) we w ere able
to relate the significance o f cockle effects to physical disturbance,
a n d to tem poral changes in the presence o f species life stages a n d
likely changes in cockle behavior.
Firstly, w e dem onstrate the tem p o ral d ependence o f the strength
a n d outcom e o f cockle effects on physical a n d biological sedim ent
properties. W e suggest two aspects as bein g governing drivers o f
the observed tem p o ral effect: (1) species-specific life-stage d e p en ­
d e n t vulnerability to cockle interference, a n d (2) c hanging cockle
beh av io r associated w ith increasing SSC. W e found reduced
densities o f the d o m in a n t surface-dw elling species w hen cockles
w ere p re sen t in the cohesive sedim ents. L ow er densities m ay have
resulted from b o th direct interference com petition a n d active postsettlem ent dispersal [29,30]. T h e absence o f a n effect o f cockle
rem oval o n the subsurface-dw elling O ligochaeta spp. a n d H.
filiformis suggests th a t cockle effects o n b e n th ic com m unities in
cohesive sedim ents are m ainly m ed iated by interference effects o f
cockle b io tu rb a tio n in the surface sedim ent layer. F u rth erm o re,
densities o f the L D S D F A. marioni a n d P. elegans w ere num erically
less red u ced in the C plots d u rin g the p o st-recru itm en t trial, th an
d u rin g the re cru itm e n t trial w hich suggests th a t larvae a n d
recently recru ited juveniles o f these species are m ore vulnerable to
cockle interference as c o m p a red to 4—5 m onths old juveniles. T his
is particularly clear for A. marioni w hich was red u ced by 35%
d u rin g the re cru itm e n t trial, w hile the p o p u latio n density o f this
species was n o t affected b y cockle presence or rem oval d u rin g the
po st-recru itm en t trial. T his species has a direct larval benthic
developm ent (w w w .m arlin.ac.uk) a n d is thus potentially highly
vulnerable to d isturbance o f the sedim ent d u rin g its larval stage.
A verage suspended sedim ent concentrations increased a t the
Cockle effects in cohesive sedim ents
M ed ian grain size decreased d u rin g the po st-recru itm en t trial,
in d ep e n d en t o f cockle tre a tm e n t (Figure 2). Cockles significantly
affected physical a n d biological sedim ent properties, tho u g h the
effects often varied tem porally. C ockle presence significantly
en h an c ed C PE d u rin g the p o st-recru itm en t trial in O c to b e rN o v em b er (Figure 2) (T able S2 in File SI). F u rth e rm o re , total
m acro b en th o s a n d L D S D F density was red u ce d w hen cockles
w ere present, th o u g h this decrease was m ore p ro n o u n c ed du rin g
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June 2013 | Volume 8 | Issue 6 | e65861
Context-Dependent Cockle Effects on Benthos
A) Total benthos
E) LDSDF benthos
B) Total benthos
F) LDSDF benthos
= 0.6
S. 0.4
£,0.4
C) Total benthos
G) LDSDF benthos
2 0.8
0.6
.2 0.4
Pm
-r'a 20 -1
rt
o
o 15
d
o
o
O
Id
H) LDSDF benthos
4
£
£
2
G
10
>
&
M ay-June
Oct-Nov
cohesive
M ay-June
Oct-Nov
cohesive
o
a
o
O
2
2
O
2
non-cohesive
a
o
o
Oct-Nov
a
2
o
o
M ay-June
o
o
2
O
o
o
O
2
o
O
2
o
o
2
2
o
5 ■
o
----- 1----- 1----- 1----- 1-----
D) Total benthos
M ay-June
Oct-Nov
non-cohesive
Figure 3. S patio-tem poral effects o f cockle tre a tm e n t on biological sedim ent properties. S p e c ie s ric h n e ss, diversity, e v e n n e s s a n d to ta l
d e n s ity fo r th e to ta l c o m m u n ity (A-D) a n d th e le ss-m o b ile su rfa c e d e p o s it fe e d e r s (LDSDF, E-H); s h o w n a s m e a n ± SE fo r p lo ts w ith o u t (NC) a n d w ith
(C) c o ck les in th e tw o c o n tra s tin g s e d im e n ts d u rin g b o th e x p e rim e n ta l trials, i.e. d u rin g r e c ru itm e n t (M a y -Ju n e ) a n d p o s t-re c ru itm e n t (O c to b e rN o v e m b er). N o te th a t p r e s e n te d d e n s itie s a re s q u a re ro o t tra n s fo rm e d .
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 5 8 6 1 .g 0 0 3
cohesive study site from 4 7 .8 -5 7 .3 m g.L 1 in M a y -Ju n e to 7 3 .3 93.9 m g.L 1 in O c to b e r-N o v e m b e r (i.e. post-recruitm ent), w ith a
re co rd e d m axim um co n cen tratio n o f 165.0 m g.L 1 in N ovem ber.
T his is a yearly p h e n o m e n o n [31,32] a n d is m ost likely associated
w ith e n h an c ed rainfall a n d associated sod erosion in the Sheldt
catch m e n t a rea in this p e rio d o f the y ear [32]. C iu ta t et al. [22]
em pirically d e m o n stra ted th a t C. edule increases its frequency o f
valve clapping w ith increasing SSC in o rd e r to eject excess
sedim ents from its m an d e cavity. T his beh av io r generally increases
linearly w ith the increase in SSC until ~ 3 0 0 m g .L [22].
Populations o f P. elegans a n d juveniles o f M . balthica w ere
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significandy red u ced w hen cockles w ere p re sen t in the p erio d
w ith en h an c ed SSC a n d thus supposedly also h igher cockle
b io tu rb a tio n rates. B oth species rely substantially o n m icroalgal
carb o n for their d iet a t P aulinaschor [18,33]. H en ce, the observed
higher C P E c o n ce n tra tio n in the C plots d u rin g the post­
re cru itm e n t trial m ay therefore result from e n h an c ed cockle
b io tu rb a tio n -m ed ia te d decreases in density, a n d thus grazing
pressure, o f P. elegans a n d M . balthica. T h e tw o num erically
d o m in a n t species in the com m unity, A. marioni a n d P. elegans, thus
exhibited a different response to cockle presence du rin g the post­
re cru itm e n t trial in au tu m n . B ecause no species w ere outco m p eted
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June 2013 | Volume 8 | Issue 6 | e65861
Context-Dependent Cockle Effects on Benthos
12
250
Aphelochaeta marioni
200
Hydrobia ulvae
9 -
150
5
§
6
-
100 3
50 -
0
0
200
6
Pygospio elegans
Scoloplos armiger
150
4 -
100 2
-
50 -
{
Pygospio elegans
Oligochaeta
14 -
10 -
6
i
Heteromastus filiformis
Urothoe poseidonis
M acom a balthica (recruits)
Cerastoderma edule (recruits)
*
>
-
NC
I
*
C
NC
M a y -Ju n e
1
i
C
NC
Oct-N ov
I
C
NC
M ay -Ju n e
cohesive
I
C
Oct-Nov
non-cohesive
Figure 4. Tem po ral effects o f cockle tre a tm e n t on th e d en sity o f th e five m ost d o m in an t species per study site. D e n sities a re s h o w n as
m e a n ± SE fo r p lo ts w ith o u t (NC) a n d w ith (C) c o ck les d u rin g b o th e x p e rim e n ta l trials, i.e. d u rin g re c ru itm e n t (M a y -Ju n e ) a n d p o s t-re c ru itm e n t
(O c to b e r-N o v e m b e r) in th e c o h e s iv e s e d im e n ts (left p a n e l) a n d in th e n o n -c o h e siv e s e d im e n ts (rig h t p a n el).
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 5 8 6 1 ,g 0 0 4
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Context-Dependent Cockle Effects on Benthos
by cockles (i.e. total species n u m b e r re m a in e d co n stan t in C a n d
N C plots) bu t, o f the two species, only P. elegans was inhibited by
cockle presence du rin g the po st-recru itm en t trial, evenness a n d
diversity decreased d u rin g this trial.
Secondly, o u r study dem onstrates the poten tial for physical
d isturbance resulting from h ydrodynam ic forces to overw helm the
effects o f cockles on physical a n d biological sedim ent properties.
A bove a threshold, physical factors are considered relatively m ore
im p o rta n t th a n biotic interactions in m ediating com m unity
o rganization (e.g. [34,35]). T h o u g h C. edule clearly has the
potential to affect its physical a n d biological environm ent, we
conclude th a t the physical d isturbance o f the sedim ent b e d
associated w ith h ydrodynam ic forces a t the non-cohesive study
site, w hich has consequences for organism dispersal a n d species
pop u latio n dem ographics [15,36], likely obliterated the ecosystem
engineering o f C. edule on the surface sedim ent layers. In general,
differences in b enthic biological c om m unity attributes a n d physical
sedim ent properties w ere greater betw een the two contrasting
sedim ent types du rin g b o th e x perim ental trials, th a n betw een
w hen cockles w ere p re sen t o r rem oved (Figures 2, 3). T his
illustrates th a t physical d isturbance resulting from w ave action a n d
tidal currents is a governing process o f estuarine b enthic diversity
a n d sedim ent p roperties (e.g. [18,37]). T h e stability o f b e d
sedim ent depends on the balance betw een h ydrodynam ic forces
th a t cause erosion a n d the forces w ithin the sedim ent th a t resist it,
w ith consolidated sedim ent th a t c o n ta in fine particles (e.g. m ud,
i.e. particles < 6 3 pm) typically h aving a low er propensity to be
ero d ed th en unconsolidated, non-cohesive sedim ents (G rabow ski
et al. [38], a n d references therein).
In conclusion, o u r results em phasize th a t physical d isturbance o f
the sedim ent b e d due to h y drodynam ic forcing, can constrain the
outcom e o f biotic interactions a t the local scale, a n d th a t tem poral
changes in e nvironm ental stressors, e.g. suspended sedim ent
concentrations, m ay affect the outcom e o f key species interference
effects, e.g. th ro u g h changes in key species b ehavior a n d life-stage
specific vulnerability to interference from b io tu rb atio n . As a
consequence, the o b tain e d results suggest th a t inconsistencies
a m o n g previous studies th a t exam ined the effect o f cockle loss or
m an ip u lated cockle densities on b enthic com m unities (see e.g. [3 9 41]) m ay result from differences in the strength a n d outcom e o f
interference effects d ep en d in g o n the spatial a n d tem poral context.
E xperim ents c o n d u cted a t m ultiple sites a n d tim es should
therefore b e considered preferable in o rd e r to generalize results
o f how key species affect ecosystem properties [42], therew ith
e n h an cin g o u r u n d e rstan d in g o f ecosystem resilience in the
context o f spatio-tem poral variable stressors. C onsequendy, the
o b tain e d insights into the c o n tex t-d ep en d en t effects o f cockles on
biotic a n d abiotic sedim ent properties in this study are relevant to
assess shallow coastal ecosystem stability, in p a rticu la r for those
systems th a t are subjected to c hanging sedim ent dynam ics. T his
study illustrates th a t processes th a t alter b e d shear stress a n d
sedim ent lo ad in coastal cohesive soft-sedim ent systems (e.g.
changes in hydro-m orphology, storm frequency a n d intensity,
terrigeneous sedim ent run-off, etc.) will affect cockle-m ediated
influences o n ecosystem properties, im p airin g the resilience o f
ecosystem functioning.
Supporting Information
F ile S I Figure S I, L ocation o f the study sites (transect lines in
white) in the m id intertidal zone a t Paulinaschor a n d V iane, a n d
locations for m onthly sam plings o f suspended sedim ent con cen ­
trations (red circles) in the subtidal channel. T ab le S I, T hree-w ay
factorial p e rm u tatio n al a n o v a results o f the effect o f plot
incubation (Factor: L ocation, i.e. in o r o u t the plot) o n physical
(water content, chloroplastic p h o to p ig m e n t equivalent c o n ce n tra ­
tions, m ed ia n grain size) a n d biological (com m unity structure)
sedim ent p roperties a t the two sites (Factor: Site) for the two
experim ental trials (Factor: Trial). Boldfaced p-values indicate
significant effect a t p < 0 .0 5 . T ab le S2, T w o-w ay factorial analysis
o f v ariance results (p-values) o f the effect o f cockle rem oval or
presence (Factor: T reatm en t) on physical a n d biological sedim ent
p roperties d u rin g the two experim ental trials (Factor: Trial) a t the
cohesive study site. B oldfaced p-values indicate significant effect at
p < 0 .0 5 . T ab le S3, T w o-w ay factorial analysis o f v ariance results
(p-values) o f the effect o f cockle rem oval or presence (Factor:
T reatm en t) o n physical a n d biological sedim ent p roperties du rin g
the two e x perim ental trials (Factor: T rial) a t the non-cohesive
study site. presults from p erm u tatio n al analysis o f variance.
B oldfaced p-values indicate significant effect a t p < 0 .0 5 .
(D O C X )
Acknowledgm ents
W e thank Jero en V an D aelen, Jo s V an Soelen, Douwe van den Ende,
M ershad T aheri, Elisabeth Debusschere, Niels Viane, Bart Beuselinck,
Anne Willems, L ander B lom m aert and Eline R em ue for assistance in the
fieldwork. Ju rg en V erstraeten is acknowledged for construction o f the
incubation frames and Dirk V an Gansbeke and B art Beuselinck for
execution o f the physico-chemical analyses.
Author Contributions
Conceived and designed the experiments: C V C TY SFT. Perform ed the
experiments: C V C . Analyzed the data: C V C . C ontributed reagents/
m aterials/analysis tools: C V C M V TY. W rote the paper: C V C SFT M V
TY.
References
1. G o s ta n z a R , d A rg e R , d e G r o o t R , F ä r b e r S, G ra sso M , e t al. (1997) T h e v a lu e o f
th e w o r ld ’s e c o sy ste m services a n d n a tu r a l c a p ita l. N a tu r e 387: 2 5 3 —260.
7.
2.
o f tw o c o n tra s tin g c o m m u n ity ty p es. M a rin e E co lo g y -P ro g ress S eries 307: 115—
125.
8. W o o d in SA , W e th e y D S , H e w itt J E , T h r u s h S F (2012) S m a ll scale te rre s tria l
c lay d e p o sits o n in te rtid a l san d flats: B e h a v io ra l c h a n g e s a n d p ro d u c tiv ity
re d u c tio n . J o u r n a l o f E x p e rim e n ta l M a rin e B io lo g y a n d E c o lo g y 413: 184—191.
S n e lg ro v e P V R (1 9 9 9 ) G e ttin g to th e b o t to m o f m a r in e b io d iv e rsity :
S e d im e n ta ry h a b ita ts - O c e a n b o tto m s a re th e m o s t w id e s p re a d h a b ita t o n
E a r th a n d s u p p o rt h ig h b io d iv e rsity a n d k ey e co sy stem services. B io scien ce 49:
1 2 9 -1 3 8 .
3. A iro ld i L. B eck M W (2007) Loss, s ta tu s a n d tre n d s fo r c o a sta l m a r in e h a b ita ts o f
E u ro p e . O c e a n o g r a p h y a n d M a rin e B iology, V o l 45 45: 3 4 5 -4 0 5 .4 .
4.
5.
6.
9. N a v a r ro J M , W id d o w s J (1997) F e e d in g p h y sio lo g y o f C e r a s to d e rm a e d u le in
L o tz e H K , L e n ih a n H S , B o u rq u e BJ, B ra d b u ry R H , C o o k e R G , e t al. (2006)
D e p le tio n , d e g ra d a tio n , a n d rec o v e ry p o te n tia l o f e stu a rie s a n d c o a sta l seas.
res p o n s e to a w id e r a n g e o f se sto n c o n c e n tra tio n s. M a rin e E c o lo g y -P ro g ress
S eries 152: 1 7 5 -1 8 6 .
10. J o n e s C G , L a w to n J H , S h a c h a k M (1994) O rg a n is m s as E c o sy ste m E n g in e ers.
Sc ien c e 312: 1 8 0 6 -1 8 0 9 .
T h r u s h S F, H e w itt J E , C u m m in g s V , Ellis J I , H a tto n G , e t al. (2004) M u d d y
w a te rs: e le v a tin g s e d im e n t in p u t to c o a sta l a n d e s tu a rin e h a b ita ts . F ro n tie rs in
E c o lo g y a n d th e E n v iro n m e n t 2: 2 9 9 —306.
11.
R o d il IF , L o h re r A M , G h ia ro n i L D , H e w itt J E , T h r u s h SF (2011) D is tu rb a n c e
O ik o s 69: 3 7 3 -3 8 6 .
B ra e c k m a n U , V a n C o le n C , S o e ta e rt K , V in c x M , V a n a v e rb e k e J (2011)
C o n tr a s tin g m a c r o b e n th ic activ ities d ifferen tially a ffe c t n e m a to d e d e n sity a n d
d iv ersity in a sh a llo w su b tid a l m a r in e se d im e n t. M a rin e E co lo g y -P ro g ress S eries
4 2 2 : 1 7 9 -1 9 1 .
o f sa n d fla ts b y th in te rrig e n o u s s e d im e n t d ep o sits: c o n s e q u e n c e s fo r p r im a ry
p r o d u c tio n a n d n u trie n t cycling. E c o lo g ic a l A p p lic a tio n s 21: 4 1 6 —T26.
PLOS ONE I www.plosone.org
L o h r e r A M , T h r u s h S F, L u n d q u is t C J , V o p e l K , H e w itt J E , e t al. (2006)
D e p o s itio n o f te rrig e n o u s s e d im e n t o n su b tid a l m a r in e m a c ro b e n th o s : resp o n se
7
June 2013 | Volume 8 | Issue 6 | e65861
Context-Dependent Cockle Effects on Benthos
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
T h r u s h S F, H e w it tJ E , L o h r e r A M (2012) In te r a c tio n n e tw o rk s in c o a sta l softs e d im e n ts h ig h lig h t th e p o te n tia l fo r c h a n g e in ec o lo g ic al resilien ce. E co lo g ical
A p p lic a d o n s 22: 1 2 1 3 -1 2 2 3 .
N o rk k o A , H e w it tJ E , T h r u s h SF, F u n n e ll G A (2006) C o n d itio n a l o u tc o m e s o f
fac ilita tio n b y a h a b ita t-m o d ify in g s u b tid a l b iv alv e. E c o lo g y 87: 2 2 6 —234.
T h r u s h SF, H e w ittJ E , C u m m in g s V J, G re e n M O , F u n n e ll G A , e t al. (2000) T h e
g e n e ra lity o f field e x p e rim e n ts : I n te ra c tio n s b e tw e e n lo c a l a n d b ro a d -s c a le
p rocesses. E c o lo g y 81: 39 9 —41 5 .
H u n t H L (2004) T r a n s p o r t o f ju v e n ile clam s: effects o f sp ecies a n d s e d im e n t
g ra in size. J o u r n a l o f E x p e rim e n ta l M a rin e B iology a n d E c o lo g y 312: 2 7 1 —284.
V a n C o le n G , M o n ts e r ra t F, V in c x M , H e r m a n P M J, Y s e b a e rt T , e t al. (2010)
L o n g -te rm d iv e rg e n t tid a l fla t b e n th ic c o m m u n ity re c o v e ry fo llo w in g h y p o x iain d u c e d m o rta lity . M a rin e P o llu tio n B u lle tin 60: 178—186.
G a m M , d e M o n ta u d o u in X , B a z a iri H (2010) P o p u la tio n d y n a m ic s a n d
s e c o n d a ry p r o d u c tio n o f th e co ck le C e r a s to d e rm a ed u le: A c o m p a ris o n b e tw e e n
M e rja Z e rg a { M o ro c c a n A d a n tic C o a st) a n d A r c a c h o n B ay {F ren ch A d a n tic
C oast). J o u r n a l o f S ea R e s e a rc h 63: 191—201.
V a n C o le n C , M e u le p a s G , D e B a c k e r A , v a n d e r W a l D , V in c x M , e t al. {2010)
D iv e rsity , tr a it d isp la c e m e n ts a n d shifts in a sse m b la g e s tru c tu re o f tid a l fla t
d e p o s it fee d e rs a lo n g a g r a d ie n t o f h y d ro d y n a m ic stress. M a rin e E c o lo g y
P ro g re ss S eries 406: 7 9 -8 9 .
T r o o s t K , K a m e rm a n s P, W o lff W J {2008) L a rv ip h a g y in n a tiv e b iv alv es a n d a n
in tr o d u c e d oyster. J o u r n a l o f S ea R e s e a rc h 60: 157—163.
R o ssi F , G rib sh o lt B, M id d e lb u rg J J , H e ip C {2008) C o n te x t- d e p e n d e n t effects o f
s u sp e n sio n fe e d in g o n in te r d d a l e co sy stem fu n c tio n in g . M a rin e E c o lo g y -P ro g ress
S eries 354: 4 7 - 5 7 .
M o n ts e r ra t F , V a n C o le n C , P r o v o o s t P , M illa M , P o n ti M , e t al. {2009)
S e d im e n t s e g re g a d o n b y b io d iffu sin g b ivalves. E s tu a rin e C o a s ta l a n d S h e lf
C la rk e K R , G o rle y R N {2006) P rim e r v6: U s e r m a n u a l/tu to r ia l. P rim e r-E ,
P ly m o u th M a rin e L a b o ra to ry , P ly m o u th , U .K .
28.
A n d e rs o n M J , G o rle y R N , C la rk e K R {2008) P e r m a n o v a + fo r p rim e r: g u id e to
so ftw a re a n d statistic a l m eth o d s . P rim e r-e : P ly m o u th , U K .
29.
H id d in k J G , K o c k R P , W o lff W J {2002) A ctiv e p e la g ic m ig ra d o n s o f th e bivalve
30.
M a c o m a b a lth ic a a re d a n g e ro u s . M a rin e B iology 140: 1149—1156.
V a n C o le n C , L e n o ir J , D e B a c k e r A , V a n e ls la n d e r B, V in c x M , e t al. {2009)
S e td e m e n t o f Macoma balthica la rv a e in resp o n se to b e n th ic d ia to m film s. M a rin e
31.
C h e n M S , W a rte l S, V a n E ck B, V a n M a ld e g e m D {2005) S u s p e n d e d m a tte r in
th e S h e ld t e stu ra ry . H y d ro b io lo g ia 540: 7 9 -1 0 4 .
33.
V a n C o le n C , M o n ts e r ra t F , V in c x M , H e r m a n P M J, Y s e b a e rt T , e t al. {2010)
M a c r o b e n th o s r e c r u itm e n t success in a tid a l flat: fe e d in g tr a it d e p e n d e n t effects
o f d is tu rb a n c e h isto ry . J o r u n a l o f E x p e r im e n ta l M a rin e B io lo gy a n d E c o lo g y
385: 7 9 -8 4 .
M e n g e B A , S u th e rla n d J P {1987) C o m m u n ity R e g u la d o n - V a r ia d o n in
D is tu rb a n c e , C o m p e d tio n , a n d P r e d a tio n in R e la tio n to E n v iro n m e n ta l-S tre ss
a n d R e c ru itm e n t. A m e ric a n N a tu ra lis t 130: 7 30—757.
35.
36.
37.
38.
39.
B e rtn e ss M D , C a lla w a y R {1994) Po sitiv e In te r a c tio n s in C o m m u n itie s . T r e n d s
in E c o lo g y & E v o lu tio n 9: 191—193.
C o m m ito J A , T h r u s h S F, P rid m o r e R D , H e w itt J E , C u m m in g s V J {1995)
D is p e rs a l d y n a m ic s in a w in d - d r iv e n b e n th i c s y s te m . L im n o lo g y a n d
O c e a n o g r a p h y 40: 1 5 1 3 -1 5 1 8 .
L e H ir P , R o b e rts W , C a z a ille t O , C h ristie M , B a so u lle t P , e t al. {2000)
C h a r a c te riz a tio n o f in te rtid a l f la t h y d ro d y n a m ic s . C o n tin e n ta l S h e lf R e s e a rc h
20: 1 4 3 3 -1 4 5 9 .
G ra b o w sk i R C , D ro p p o I G , W h a r to n G {2011) E ro d ib ility o f c o h e siv e se d im e n t:
T h e im p o r ta n c e o f s e d im e n t p ro p e rtie s . E a rth -S c ie n c e R ev iew s 105: 101—120.
F la c h E C {1996) T h e in flu e n ce o f th e cockle, C e r a s to d e rm a e d u le , o n th e
m a c ro z o o b e n th ic c o m m u n ity o f tid a l flats in th e W a d d e n Sea. M a rin e E cologyP u b b lic a z io n i D e lla S ta z io n e Z o o lo g ic a D i N a p o li 1 17: 8 7 —98.
40.
C e s a r C P , F r id C L J {2009) E ffe c ts o f e x p e rim e n ta l s m a ll-s c a le co c k le
{ C e ra s to d e rm a e d u le L.) fish in g o n e c o sy ste m fu n ctio n . M a rin e E c o lo g y -a n
E v o lu tio n a ry P e rsp e c tiv e 30: 123—137.
41.
W ijn h o v e n S, E s c a v a ra g e V , H e r m a n P M J , S m a a l A , H u m m e l H {2011) S h o r t
a n d m id -lo n g te r m effects o f c o c k le -d re d g in g o n n o n - ta r g e t m a c ro b e n th ic
species: a b e fo re -a fte r-c o n tro l im p a c t e x p e rim e n t o n a tid a l m u d fla t in th e
O o s te rs c h e ld e {The N e th e rla n d s). M a rin e E c o lo g y 32: 1—13.
H e w it tJ E , T h r u s h SF, D a y to n P K , B o n s d o rf E {2007) T h e effect o f s p a tia l a n d
te m p o r a l h e te ro g e n e ity o n th e d e sig n a n d an aly sis o f e m p iric a l stu d ie s o f scaled e p e n d e n t system s. T h e A m e ric a n N a tu ra lis t 169: 398M 4J8.
42.
8
B io lo g y 156: 2 1 6 1 -2 1 7 1 .
V a n D a m m e S, S tru y f E , M a ris T , Y s e b a e rt T , D e h a irs F, e t al. {1995) S p a d a l
a n d te m p o r a l p a tte rn s o f w a te r q u a lity a lo n g th e e stu a rin e salin ity g r a d ie n t o f th e
S c h e ld t e s tu a ry {B elgium a n d th e N e th e rla n d s): resu lts o f a n in te g r a te d
m o n ito rin g a p p ro a c h . H y d ro b io lo g ia 540: 26—45.
32.
34.
S c ien c e 83: 3 7 9 -3 9 1 .
C iu ta t A , W id d o w s J , P o p e N D {2007) E ffe c t o f C e r a s to d e rm a e d u le d e n sity o n
n e a r- b e d h y d ro d y n a m ic s a n d sta b ility o f c o h e siv e m u d d y se d im e n ts. J o u r n a l o f
E x p e r im e n ta l M a rin e B io lo g y a n d E c o lo g y 346: 114—126.
T h r u s h SF, H e w itt J E , D a y to n P K , C o c o G , L o h r e r A M , e t al. {2009)
F o re c a s tin g th e lim its o f resilien ce: in te g ra tin g e m p iric a l re s e a rc h w ith th eo ry .
P ro c e e d in g s o f th e R o y a l S o ciety B 276: 3 2 0 9 -3 2 1 7 .
C o o s e n J , Seys J , M e ire P M , C ra y m e e rs c h J A M {1994) Effects o f se d im e n to log ic a l a n d h y d ro y d n a m ic a l c h a n g e s in th e in te rtid a l a re a s o f th e O o s te rs c h e ld e
e s tu a ry {SW N e th e rla n d s) o n d is trib u tio n , d e n sity a n d b io m a ss o f five c o m m o n
m a c r o b e n th ic species: S pio m a rtin e n s is {M esnil), H y d r o b ia u lv ae { P ennant),
A r e n ic o la m a r in a {L.), S c o lo p lo s a rm ig e r {M uller) a n d B a th y p o re ia sp.
H y d ro b io lo g ia 282:2 8 3 : 2 3 5 -2 4 9 .
V a n C o le n C , M o n ts e r ra t F, V in c x M , H e r m a n P M J, Y s e b a e rt T , e t al. {2008)
M a c r o b e n th ic re c o v e ry f ro m h y p o x ia in a n e s tu a rin e tid a l m u d fla t. M arine ecology
progress series 372: 31—42.
J e ffre y S W , M a n to u r a R F C , W rig h t S W {1997) P h y to p la n k to n p ig m e n ts in
o c e a n o g ra p h y . U n ite d N a tio n s I n te r n a tio n a l, P a ris
PLOS ONE I www.plosone.org
27.
June 2013 | Volume 8 | Issue 6 | e65861