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Influence of suspended scallop cages and mussel
lines on pelagic and benthic biogeochemical
fluxes in Havre-aux-Maisons Lagoon,
Îles-de-la-Madeleine (Quebec, Canada)
Marion Richard, Philippe Archambault, Gérard Thouzeau, Chris W. McKindsey,
and Gaston Desrosiers
Abstract: An in situ experiment was done in July 2004 to test and compare the influence of suspended bivalve cultures
(1- and 2-year-old blue mussels (Mytilus edulis) and sea scallops (Placopecten magellanicus)) on biogeochemical fluxes in
the water column and at the benthic interface in Havre-aux-Maisons Lagoon (Quebec, Canada). Aquaculture structures in-
creased the pelagic macrofaunal biomass (PMB) and acted as an oxygen sink and nutrient source in the water column un-
der dark conditions. Although PMB was lower in scallop culture, the influence of scallop cages on pelagic fluxes was
similar to or greater (nitrate and nitrite) than that of mussel lines. Sediments were organically enriched, and benthic
macrofaunal abundances were decreased in mussel culture zones relative to the control zone, but such an effect was not
observed in the scallop zone. Nevertheless, benthic oxygen demand did not vary among culture types and control zones.
Benthic nutrient fluxes were greatest beneath aquaculture structures. Both pelagic and benthic interfaces may modify oxy-
gen and nutrient pools in culture zones in Havre-aux-Maisons Lagoon. The contribution of aquaculture structures to oxy-
gen, ammonium, and phosphate pools may be a function of PMB and type. While aquaculture structures had an important
role on nitrate and nitrite cycling, silicate turnover was mainly driven by benthic mineralization of biodeposits.
Résumé : Une série d’expériences in situ a été réalisée en juillet 2004 afin de tester et de comparer l’influence de cultu-
res de bivalves en suspension (moules (Mytilus edulis)de1anetde2ansetpétoncles(Placopecten magellanicus)) sur
les flux biogéochimiques dans la colonne d’eau et à l’interface eau-sédiment dans la lagune du Havre-aux-Maisons (Qué-
bec, Canada). Les structures aquacoles augmentent la biomasse de la macrofaune pélagique (PMB) et agissent comme un
puits d’oxygène et une source de nutriments dans la colonne d’eau en condition d’obscurité. Bien que la PMB soit plus
faible au niveau de la pectiniculture, l’influence des paniers de pétoncles sur les flux pélagiques est similaire, voire supé-
rieure (nitrates et nitrites), à celle des filières de moules. Au contraire de la pectiniculture, les cultures de moules enrichis-
sent le sédiment en matière organique et diminuent l’abondance des organismes benthiques par comparaison aux zones
témoins. Cependant, la demande benthique en oxygène ne varie pas entre les différentes zones de culture et les zones
témoins. Les flux benthiques de sels nutritifs atteignent un maximum sous les structures aquacoles. L’interface benthique
et l’interface pélagique modifient potentiellement les stocks d’oxygène et de sels nutritifs dans les zones de cultures de la
lagune du la lagune du Havre-aux-Maisons. La contribution des structures aquacoles aux stocks d’oxygène, d’ammonium
et de phosphates pourrait dépendre de la PMB et du type des bivalves en culture. Alors que les structures aquacoles
jouent un rôle important dans le cycle des nitrates et des nitrites, le cycle du silicium est régi principalement par la miné-
ralisation benthique des biodépôts.
Richard et al. 1505
Can. J. Fish. Aquat. Sci. 64: 1491–1505 (2007) doi:10.1139/F07-116 © 2007 NRC Canada
1491
Received 20 September 2006. Accepted 7 June 2007. Published on the NRC Research Press Web site at cjfas.nrc.ca on 19 October
2007.
J19546
M. Richard, P. Archambault,1,2 and C.W. McKindsey. Sciences de l’Habitat, Institut Maurice Lamontagne, Pêches et Océans
Canada, 850 route de la mer, P.O. Box 1000, Mont Joli, QC G5H 3Z4, Canada.
G. Thouzeau. Centre national de la recherche scientifique (CNRS), Unité mixte de recherche (UMR) 6539, Institut Universitaire
Européen de le Mer, Technopôle Brest Iroise, place Nicolas Copernic, 29280 Plouzané, France.
G. Desrosiers.3Institut des Sciences de la Mer, Université du Québec à Rimouski, 310 allée des Ursulines, C.P. 3300, Rimouski,
QC G5L 3A1, Canada.
1Corresponding author (e-mail: philippe_archambault@uqar.qc.ca)
2Present address: Institut des Sciences de la Mer, Université du Québec à Rimouski, 310 allée des Ursulines, C.P. 3300, Rimouski,
QC G5L 3A1, Canada.
3Deceased.
Introduction
Structures used in suspended bivalve aquaculture, such as
longlines or cages, provide substrates for both cultivated and
biofouling organisms in the water column (Lesser et al.
1992; Claereboudt et al. 1994; McKindsey et al. 2006). Over
time, organic matter accumulates within the structure, and
the abundance and biomass of the associated organisms in-
crease (Taylor et al. 1997; Mazouni et al. 2001; Richard et
al. 2006). Only four studies have examined the influence of
this novel suspended benthic interface on biogeochemical
fluxes in the water column (i.e., Leblanc et al. 2003;
Mazouni 2004; Nizzoli et al. 2006; Richard et al. 2006), al-
though the metabolism of cultivated bivalves and their asso-
ciated fauna as well as the degradation of associated organic
matter have been shown to increase oxygen consumption
and nutrient releases in the adjacent water (Richard et al.
2006).
Biodeposition by cultivated bivalves has been shown to
organically enrich sediments (Grenz et al. 1990; Deslous-
Paoli et al. 1998; Stenton-Dozey et al. 2001), which has
been shown to increase oxygen consumption and nutrient
fluxes at the water–sediment interface (Baudinet et al. 1990;
Hatcher et al. 1994; Christensen et al. 2003). Organic en-
richment and decreased oxygen concentrations may lead to
less diverse benthic communities (Pearson and Rosenberg
1978; Nilsson and Rosenberg 2000; Gray et al. 2002). Since
benthic community metabolism depends partly on macro-
faunal biomass (Mazouni et al. 1996) and abundance
(Nickell et al. 2003; Welsh 2003), any change in macro-
faunal biomass or abundance may influence benthic bio-
geochemical fluxes.
Aquaculture structures contain a great biomass of macro-
fauna, whereas the benthic interface is largely dominated by
the mass of sediments. Owing to their different compositions,
biogeochemical processes may vary between interface types
and lead to contrasting nutrient release ratios (e.g., Si/N/P).
Disequilibria in nutrient release kinetics can alter the original
nutrient ratios and thus the specific composition of phyto-
plankton communities (Baudinet et al. 1990). Thus, the two
interfaces may have different influences on phytoplankton
community composition. The contribution of the pelagic inter-
face to these pools is likely to be a function of the density of
aquaculture structures as well as their composition (bivalve size
and species, associated organisms, detritus, etc.).
The aim of this study was to examine and compare the in-
fluence of suspended bivalve culture on oxygen and nutrient
pools and nutrient ratios in a semi-enclosed lagoon. Spe-
cifically, we used in situ mensurative experiments (sensu
Hulbert 1984) to evaluate oxygen and nutrient fluxes at both
the pelagic (i.e., aquaculture structure) and benthic (sedi-
ment) interfaces associated with all types of aquaculture be-
ing practiced in the studied lagoon (i.e., sea scallops
(Placopecten magellanicus Gmelin) in pearl nets and 1- and
2-year-old blue mussels (Mytilus edulis L.) on longlines).
This study is the first to test the influence of suspended scal-
lop culture and one of the few studies to compare benthic
and pelagic influences of suspended bivalve cultures
(Mazouni 2004; Nizzoli et al. 2006). For efficacy, we use the
term flux when discussing either oxygen consumption (i.e.,
decreasing oxygen concentration) or nutrient generation
(i.e., increasing nutrient concentration). Several factors asso-
ciated with bivalve culture (organic matter, associated
macrofaunal assemblages) were also evaluated to better un-
derstand the mechanisms involved.
More specifically, three hypotheses were evaluated in this
study: (i) the introduction of suspended aquaculture struc-
tures increases biogeochemical fluxes in the water column;
(ii) sediment organic matter content, macrofaunal abun-
dance, and fluxes are greater at the benthic interface in cul-
ture zones than in a control zone, whereas the opposite is
true with respect to macrofaunal biomass; and (iii) ratios of
nutrient releases and the contribution to oxygen and nutrient
pools differ between interfaces, such that pelagic interfaces
consume more oxygen and produce more nitrogen and phos-
phate, whereas benthic interfaces produce more silicate. We
further predict that both the benthic and pelagic influences
of 2-year-old mussel lines would be greater than those of
1-year-old mussel lines and scallop cages, as their biomass
was greatest.
Materials and methods
Study area
The study was done in the Îles-de-la-Madeleine archipel-
ago located in the Gulf of St. Lawrence, eastern Canada
(Fig. 1a). The study area was the Havre-aux-Maisons La-
goon (HAM) located in the central part of the archipelago
(47°26′N, 61°50′W; Fig. 1b). The surface area of HAM is
30 km2(Comité ZIP des Îles 2003). HAM is linked to the
Gulf of St. Lawrence in the southeast and to the Grande-
Entrée Lagoon in the northeast (Fig. 1b). As in Grande-
Entrée Lagoon, rainfall is the only source of fresh water to
HAM because of the absence of rivers (Souchu and
Mayzaud 1991). Tides are small (mean of 0.58 m;
Koutitonsky et al. 2002). As observed in Grande-Entrée
Lagoon (Souchu et al. 1991), shallow water (maximum
depth of 6 m) and frequent winds up to 15 m·s–1 (Souchu et
al. 1991) may lead to water column mixing. Over the course
of the study in July 2004, the mean (± standard error, SE)
salinity, temperature, and oxygen concentration were
30.83 ± 0.02 psu, 19.07 ± 0.14 °C, and 7.1 ± 0.13 mg·L–1,
respectively. The mean chlorophyll aconcentration (± stan-
dard deviation, SD) measured in the summer 2004 was 1.90 ±
1.09 µg·L–1 (May to September; G. Tita, Centre de recherche sur
les milieux insulaires et maritimes (CERMIM), 37 Chemin Cen-
tral, Havre-aux-Maisons, Îles-de-la-Madeleine, QC G4T 5P4,
Canada, guglielmo_tita@uqar.qc.ca, unpublished data).
Study shellfish cultures
HAM has been exploited for blue mussel culture since the
1980s. In 2004, mussel cultures were located in the central
portion of the lagoon (Fig. 1c). In 2004, the annual produc-
tion was 160 tonnes, and the farm surface area was 1.25 km2
(A. Huet, Moules de culture des Iles, 721 chemin Gros-Cap,
Étang du Nord, Îles-de-la-Madeleine, QC G4T 3M5,
mciaqua@tlb.sympatico.ca, personal communication). The
mussel grow-out cycle is approximately 2 years. For practi-
cal reasons, the 1-year-old (M1) and the 2-year-old (M2)
mussel longlines were deployed in two distinct zones
(Fig. 1c). Mussels were cultivated on 244 m long suspended
mussel lines that are deployed in loops and attached to 76 m
© 2007 NRC Canada
1492 Can. J. Fish. Aquat. Sci. Vol. 64, 2007
long horizontal longlines anchored in the sediment at each
end. These mussel longlines were separated from each other
by 12 m (A. Huet, personal communication). In July 2004,
there were 200 lines for M1 mussels and 40 lines for M2
mussels in the lease area, as most of the latter had already
been harvested (A. Huet, personal communication). At that
time, the density of mussel lines, expressed as the length of
mussel sock per square metre of culture area (where mussel
lines were still present, was 26 cm·m–2 in both mussel zones.
The sea scallop has also been cultivated on suspended
longlines in HAM since the end of the 1990s to seed juve-
niles for scallop fishery areas located in the Gulf of St. Law-
rence (Cliche and Guiguère 1998). The scallop culture zone
(S) was located in the southeast portion of the lagoon
(Fig. 1c). In fall 2003, juvenile scallops from collectors were
transferred to pearl nets. Each of these pyramidal-shaped
cages contained 100–150 scallops (shell size: 7–25 mm;
D. Hébert, CultiMer, 55 route 199, Fatima, Iles-de-la-
Madeleine, QC G4T 2H6, petoncle@tlb.sympatico.ca, per-
sonal communication). Cages were stacked in series of five
and hung from the same type of longlines as used in mussel
culture. One hundred and twenty-five of these stacks were
installed on each longline in fall 2003 (S. Vigneau,
CultiMer, 55 route 199, Fatima, Iles-de-la-Madeleine, QC
G4T 2H6, petoncle@tlb.sympatico.ca, personal communica-
tion), 465 longlines supported scallop cages (≈29–44 million
scallops). In July 2004, after the spring seeding of most of
the scallops, only seven lines still had pearl nets (S.
© 2007 NRC Canada
Richard et al. 1493
Fig.1. Location of study area: (a) Gulf of St. Lawrence, Canada (QC, Quebec; NB, New Brunswick; NS, Nova Scotia; NF, New-
foundland); (b) Îles-de-la-Madeleine; (c) Havre-aux-Maisons Lagoon. Polygons with solid borders show the extent of scallop and
mussel culture areas in July 2004. Ellipses correspond to scallop (S), 1 year-old mussel (M1), and 2-year-old mussel (M2) study
zones. The control zone (C) is indicated by the peripheral polygon with broken borders.
Vigneau, personal communication). At that time, the density
of scallop cages, expressed as the number of cages per
square metre of culture area (in which scallop cages were
still present), was 0.785·m–2 in S.
Experimental design
In situ experiments were performed in HAM during the
summer when biogeochemical fluxes were known to be the
greatest (Mazouni et al. 2001), such that they may lead to
anoxia and eutrophication events in extreme cases (Deslous-
Paoli et al. 1988; Gray et al. 2002). Experiments were thus
carried out between 14 and 23 July 2004 in four zones: con-
trol (C, no bivalve culture), S, M1, and M2 (Fig. 1c). In con-
trast with many authors (e.g., Grenz et al. 1992; Grant et al.
1995; Mazouni et al. 1996), we designated a peripheral con-
trol zone rather than a single, local control site to distinguish
the effect of aquaculture from the natural variability of the
studied parameters (Fig. 1c). This design is more adequate
to test the influence of given treatments (see Underwood
1997). It decreases confounding factors and the misinterpre-
tation of results. Since the influence of bivalve biodeposition
is typically considered to be restricted to a radius of 10–
40 m around the farm (Dahlbäck and Gunnarson 1981;
Mattsson and Lindén 1983; Callier et al. 2006), the control
zone was located >100 m away from the bivalve farms to
avoid or limit any potential impact of bivalve biodeposition
on the benthic environment. The depth of each study zone
was similar (5.6 ± 0.1 m).
Pelagic chambers were deployed in each study zone by
scuba divers at the mean depth of bivalve structures (3 m),
whereas benthic chambers were placed at the water–
sediment interface (Fig. 2). Pelagic chambers were main-
tained in the water column by anchoring them to the bottom
with a cement block while keeping them buoyant with Sty-
rofoam floats (Fig. 2). In the control zone, pelagic chambers
were filled only with water, since there were no aquaculture
structures in that zone. In contrast, they were filled with wa-
ter and culture structures in culture zones (a scallop cage in
S and a 15 cm mussel line section in M1 and M2). Care was
taken to ensure that the pearl nets and mussel line sections
were disturbed as little as possible during the experimental
setup, as previous work in the area (Richard et al. 2006) has
shown that organisms and sediments associated with such
structures may have an important influence on fluxes. Experi-
ments were done within each of six randomly chosen sites for
each interface (pelagic vs. benthic) within each zone (C, S,
M1, M2). Thus, a total of 48 in situ incubations were done.
Experimental chambers
Macrophytes were not observed on the sea floor or on
aquaculture structures in the study zones. Dark chambers were
used in preference to clear ones to prevent potential effects of
microphyte photosynthesis (Lerat et al. 1990) on biogeochemical
fluxes to isolate the effect of aquaculture on respiration and nu-
trient regeneration rates (Bartoli et al. 2001).
Pelagic chambers were composed of two removable
acrylic hemispheres, whereas benthic chambers (Boucher
and Clavier 1990; Richard et al. 2007; Thouzeau et al. 2007)
were composed of an acrylic tube and a removable acrylic
hemisphere (Fig. 2). The large volume of water in pelagic
(82.5 L) and benthic (55.7–72.4 L, depending on the depth
to which the base was inserted into the sediment) chambers
limited the increases of diffusive and metabolic fluxes
caused by confinement or water warming. The large size of
the benthic chambers (50 cm diameter, ~0.2 m2surface area)
was also selected to limit disturbances of biogeochemical
processes due to the insertion of the base into the sediment
(Glud and Blackburn 2002) and to minimize the effects of
spatial heterogeneity in the distribution of benthic fauna
(Balzer et al. 1983).
Each chamber was linked to an adjustable, battery-fed sub-
mersible pump and YSI 6600 probe (Fig. 2). Water flow in
each chamber was adjusted to 2 L·min–1 to mix the water in-
side the enclosures, eliminate noticeable particle resuspension,
and allow stable measurements to be recorded by the YSI
probes (Richard et al. 2006, 2007; Thouzeau et al. 2007).
Physico-chemical measurements and sample collections
Pelagic and benthic chambers were incubated for 1 and
2 h, respectively. These incubation times were selected to al-
low ammonium fluxes to be measured and to attain final ox-
ygen concentrations that were not lower than 80% of initial
concentrations (Richard et al. 2006, 2007). This was to pre-
vent hypoxic conditions from developing that could modify
macrofaunal metabolism (Mazouni et al. 1998). The YSI
probe recorded oxygen concentration (mg·L–1 ± 0.01), temper-
ature (°C ± 0.01), and salinity (psu ± 0.01) in the chamber at
1 min intervals throughout the incubation. This monitoring al-
lowed us to verify if there was any change in the experimental
conditions that could modify the biogeochemical processes in
the chambers (e.g., an increase in water temperature).
© 2007 NRC Canada
1494 Can. J. Fish. Aquat. Sci. Vol. 64, 2007
Fig. 2. Schematic of in situ deployment of pelagic and benthic
experimental systems. Both systems consisted of a dark chamber
with a port to collect water samples, YSI 6600 probe, and sub-
mersible pump connected to waterproof batteries and three hoses.
Pelagic chambers were deployed at the same depth as the bivalve
structures (~3 m), whereas benthic chambers were placed at the
water–sediment interface. The arrows indicate the direction of
water circulation in the system.
Water samples (n= 3) were collected through ports in the
chambers by scuba divers using 60 ml syringes at the start,
middle (just for benthic chambers), and end of the incuba-
tions for nutrient (ammonium, silicate, phosphate, nitrate,
and nitrite) analyses. At the end of pelagic incubations,
scuba divers opened the chambers and collected the scallop
cage or mussel line section to determine its composition
(cultivated bivalves and associated macrofauna) in terms of
biomass and abundance. At the end of benthic incubations,
the hemispheres were gently pulled off the bases and scuba
divers used 60 mL disposable syringes with the ends cut off
to collect three sediment samples for analysis of the organic
matter contained within the first 2 cm. A single larger sedi-
ment core (surface area = 262.5 cm2; Wildish et al. 2003)
was also collected by scuba divers for analysis of benthic
macrofaunal biomass and abundance. We assume that the
large core surface used to collect the benthic community
samples was representative of the whole community in the
benthic chamber.
Sample processing
Pelagic and benthic macrofauna
Aquaculture structure and benthic macrofaunal samples
were sieved through a 0.5 mm screen. Cultivated bivalves
and associated and benthic macrofauna were frozen sepa-
rately at –18 °C until processed. Abundances of the cultured
bivalves and associated and benthic macrofauna were deter-
mined. Cultured bivalves were thawed in aluminium trays in
the laboratory to retain leached water, dried at 60 °C for
72 h, and weighed so as to not underestimate their dry
weight (DW: dry weight with shells). The biomass of associ-
ated and benthic organisms was similarly obtained. Mussel
and scallop biomasses were measured to the nearest 0.1 g
with a PG 5001-S Mettler Toledo balance, whereas associ-
ated and benthic macrofaunal biomasses were measured to
the nearest 10–5 g with an AG285 Mettler Toledo balance.
Following the methods used by Mazouni et al. (1998) and
Nizzoli et al. (2006), pelagic macrofaunal biomass and abun-
dance (in-chamber biomass and abundance expressed per
15 cm mussel sock and per scallop cage) were standardized
to the in situ density of aquaculture structures in culture
zones (i.e., 26 cm of mussel lines and 0.785 cage·m–2 of la-
goon bottom in mussel and scallop zones, respectively) to
obtain in situ pelagic macrofaunal biomass and abundance
(g DW·m–2 or individuals·m–2). Benthic macrofaunal bio-
mass and abundance were similarly standardized per square
metre of lagoon bottom.
Sediment organic matter content
Sediment samples were dried at 60 °C for 72 h, weighed,
and combusted for4hat450°Ctocalculate ash-free dry
weight (AFDW; Byers et al. 1978). Sediment AFDW was
measured to the nearest 10–5 g with an AG285 Mettler To-
ledo balance. Sediment organic matter (OM) content was ex-
pressed as percent total sediment weight.
Nutrient analyses
Subsamples (10 ml) were immediately taken from each
60 mL water sample in the field to measure ammonium con-
centration using the orthophtaldialdhehyde method outlined
by Holmes et al. (1999) with an Aquafluor handheld Turner
Designs fluorimeter. The remainder of each water sample
was stored in cryovials and frozen (–80 °C) after filtering
through 0.2 µm cellulose acetate Target syringe filters. Anal-
yses for dissolved nitrate, nitrite, phosphate, and silicate
were done using a II PAA II Brann + Luebbe auto-analyser
following Tréguer and Le Corre (1975).
Flux calculation and standardization
Correction for water influence
Pelagic and benthic biogeochemical fluxes were deter-
mined either from the slopes of the linear regressions be-
tween oxygen concentration and incubation time (values
expressed as mg O2·L–1·h–1) or from changes in nutrient con-
centrations through incubation (µmol nutrients·L–1·h–1) mul-
tiplied by chamber volume (values expressed as mg·h–1 or
µmol·h–1). Water within the chambers contributes to
biogeochemical fluxes through, for example, degradation of
suspended matter and respiration of plankton. However, the
aim was to isolate the portion of the biogeochemical flux
measured in pelagic and benthic chambers that was due
uniquely to the presence of the aquaculture structures and
the benthic interface, respectively. To this end, we subtracted
the influence of water (estimated as the mean fluxes mea-
sured in the dark pelagic chamber filled with water) from the
gross fluxes measured within pelagic and benthic chambers.
The mean oxygen consumption measured in water was
0.104 mg·L–1·h–1, whereas mean nutrient fluxes were 0.0679
(NH4), –0.0004 (PO4), –0.0035 (Si(OH)4), 0.0098 (NO3),
and –0.016 (NO2)µmol·L–1·h–1.
Standardization
Fluxes were standardized to a common constant to com-
pare between interfaces (pelagic vs. benthic) in culture
zones. Gross pelagic fluxes (corrected for water influence)
were standardized to in situ pelagic macrofaunal biomass
(g DW·m–2; Mazouni et al. 1998; Mazouni 2004; Nizzoli et
al. 2006). Pelagic fluxes in culture zones were thus expressed
as mg·m–2·h–1 (O2)orµmol·m–2·h–1 (nutrients) and were
comparable with benthic fluxes (corrected for water effect)
standardized toa1m
2surface area of the bottom. To evalu-
ate the effect of pelagic macrofaunal biomass (PMB) on the
pelagic fluxes among types of aquaculture structure (S, M1,
M2), pelagic fluxes were standardized to 1 kg PMB (Nizzoli
et al. 2006). As several authors (e.g., Baudinet et al. 1990;
Balzer et al. 1983; Dame et al. 1989) have done, molar ratios
of silicate, nitrogen (ammonium + nitrate + nitrite), and
phosphate releases (i.e., Si/N/P) were calculated for each ex-
perimental chamber deployed in culture zones to obtain
mean ratios of nutrient releases per interface per zone.
Statistical analyses
A series of analyses of variance (ANOVAs) were per-
formed for each study objective. The first series of ANOVAs
was done to compare pelagic macrofaunal (bivalve, associ-
ated fauna, total fauna) biomass and abundance (Table 1)
and pelagic fluxes (ammonium, silicate, phosphate, nitrate,
and nitrite; Tables 2, 3) among culture zones (S, M1, M2).
Zone C was not included in the latter model, as suspended
aquaculture was not present in that zone. A second series of
© 2007 NRC Canada
Richard et al. 1495
ANOVAs compared sediment organic matter content, ben-
thic macrofaunal biomass and abundance (Table 4), and ben-
thic fluxes (Table 5) among the four zones (C, S, M1, and
M2). The interaction among culture zones (S, M1, and M2)
and interface types (pelagic–benthic) on ratios of nutrient re-
leases (Si/P, N/P; Table 6) and biogeochemical fluxes were
also evaluated using ANOVA (Table 7). The assumptions of
normality and homoscedasticity were evaluated using the
Shapiro–Wilk (Shapiro and Wilk 1965) and Brown–
Forsythe (Brown and Forsythe 1974) tests, respectively.
When required, data were log- or square-root-transformed to
satisfy both assumptions (details given where appropriate).
A single replicate was excluded from each of the pelagic
(M2 bivalve abundance) and benthic (C sediment organic
content) databases, as their Cook’s D influences were greater
than 4/n(n= total number of replicates; Cook and Weisberg
1982). Tukey’s HSD (honestly significant difference)
pairwise multiple comparison tests adapted to unbalanced
designs (Kramer 1956; Hayter 1984) were used to identify
the differences when a source of variation was significant
(p< 0.05). Although biogeochemical fluxes were analysed sep-
arately, they were represented in the same figure for brevity.
Results
Influence of mussel and scallop cultures on the pelagic
environment
Pelagic macrofauna
In the culture zones, suspended pelagic macrofaunal biomass
and abundance varied between 47.8 and 503.1 g DW·m–2 and
181.5 and 2408 individuals·m–2, respectively. Pelagic macro-
faunal biomass and abundance differed among culture zones
(Table 1), such that M2 > M1 > S (total faunal and cultivated
bivalve biomasses; Fig. 3a), M2 = S > M1 (associated faunal
biomass; Fig. 3b),andS>M2>M1(total faunal and associ-
ated faunal abundances; Fig. 3c). The pelogic macrofaunal bio-
mass (PMB) was mainly represented by cultivated bivalves
(86.6%–99.9%; Fig. 3a), whereas the abundance of pelagic
macrofauna was mainly represented by associated fauna (56%–
94%; Fig. 3c).
Pelagic fluxes
Pelagic oxygen fluxes were negative, whereas nutrient
fluxes were mostly positive, highlighting that oxygen con-
sumption and nutrient releases in the water column origi-
nated from the aquaculture structures (Figs. 4a–4f). The
greatest nutrient release by aquaculture structures was am-
monium, followed by phosphate, silicate, nitrate, and then
nitrite (Figs. 4b–4f). Pelagic oxygen consumption varied sig-
nificantly among culture zones (Table 2) and was twice as
great in M2 than in S (Fig. 4a). Pelagic ammonium, phos-
phate, silicate, and nitrate fluxes did not vary significantly
among culture zones (Table 2; Figs. 4b–4e). Pelagic nitrite
fluxes were more than five times greater in scallop zones
than in mussel zones (Table 2; Figs. 4g–4f).
Standardized (to 1 kg PMB) pelagic fluxes measured at
the interface of aquaculture structures varied among
aquaculture structure types (Table 3). Biogeochemical fluxes
were always significantly greater at the interface of scallop
cages than at the interface of mussel lines (except for
Si(OH)4; Table 3).
Influence of mussel and scallop cultures on the benthic
environment
Sediment OM
Sediment OM ranged from 3.4% to 36.2% and differed
among zones (Table 4). The results of the a posteriori tests
showed that the mean OM in the first 2 cm of sediment was
more than twice as great in M1 and M2 than in C and S
(Fig. 5a). OM tended to be greater in S than in C, but this
trend was not significant (Fig. 5a).
Benthic macrofauna
Benthic macrofaunal biomass ranged from to 0.2 to
142 g DW·m–2. Although the trend for biomass among
zones was C, S > M1, M2 (Fig. 5b), mean macrofaunal bio-
© 2007 NRC Canada
1496 Can. J. Fish. Aquat. Sci. Vol. 64, 2007
Variable Source df MS Fp
Biomass
Total* Zone 2 4.06 56.54 <0.0001
Error 14 0.07
Bivalve* Zone 2 4.36 59.07 <0.0001
Error 14 0.07
Associated†Zone 2 7.66 19.74 <0.0001
Error 14 0.39
Abundance
Total* Zone 2 3.68 32.13 <0.0001
Error 14 0.11
Bivalve* Zone 2 0.54 10.14 0.0019
Error 14 0.05
Associated* Zone 2 6.79 40.37 <0.0001
Error 14 0.17
*ln(x).
†%(x).
Table 1. Results of analyses of variance testing the effect of cul-
ture zone (scallops, 1-year-old mussels, 2-year-old mussels) on the
biomass and abundance of total suspended macrofauna (Total),
cultivated bivalves (Bivalve), and associated fauna (Associated). Fluxes Source df MS Fp
O2* Zone 2 0.84 4.853 0.0251
Error 14 0.17
NH4Zone 2 12 876.20 1.013 0.3883
Error 14 12 712.30
PO4* Zone 2 0.16 0.835 0.4542
Error 14 0.19
Si(OH)4* Zone 2 0.89 2.117 0.1573
Error 14 0.42
NO3Zone 2 138.28 3.238 0.0699
Error 14 42.71
NO2Zone 2 48.45 35.26 < 0.0001
Error 14 1.37
*ln(x).
Table 2. Results of analyses of variance testing the effect of cul-
ture zone (scallops, 1-year-old mussels, 2-year-old mussels) on
pelagic fluxes (O2,NH
4,PO
4, Si(OH)4,NO
3,NO
2).
mass did not vary significantly among zones (Table 4).
Benthic macrofaunal abundance ranged from 76 to 10 857
individuals·m–2 and varied significantly among zones
(Table 4), such that it was six times greater in C and S than
in the M1 and M2 (Fig. 5c).
Benthic fluxes
As observed in the water column, oxygen fluxes were
negative, indicating oxygen consumption at the benthic in-
terface (Fig. 4a). Except for nitrate fluxes, which were nega-
tive in the M1 zone, mean fluxes of the other nutrients were
positive, indicating nutrient releases from sediments
(Figs. 4b–4f). Ammonium represented the greatest release at
the benthic interface, followed by silicate, phosphate, nitrate,
and nitrite releases (Fig. 4). In contrast with oxygen con-
sumption and nitrate fluxes, ammonium, silicate, phosphate,
and nitrite fluxes varied significantly among zones (Table 5;
Fig. 4). Mean ammonium, silicate, and phosphate fluxes
were 2.5–4.5 times greater in culture zones (S, M1, and M2)
than in the control zone (C; Figs. 4b–4d). Benthic ammo-
nium fluxes did not vary among culture zones (Fig. 4b). In
contrast, mean silicate and phosphate fluxes were greater in
M1 than in M2 (Figs. 4c,4d). Mean nitrite fluxes were more
than seven times greater at the water–sediment interface in S
than in M1 and M2 (Fig. 4f).
Pelagic vs. benthic interfaces
Ratio of nutrient releases
The mean release ratio of silicate to phosphate (Si/P) dif-
fered significantly between interfaces (Table 6) and was
greater at the benthic interface than at the interface of
aquaculture structures. In contrast, mean release ratios of ni-
trogen to phosphate (N/P) did not differ among culture zones
and interfaces (Table 6). The mean release ratio among sili-
cate, nitrogen, and phosphate (Si/N/P) was thus 0.62/13.11/1
at the pelagic interface and 8.34/13.11/1 at the benthic inter-
face.
© 2007 NRC Canada
Richard et al. 1497
O2NH4PO4* Si(OH)4NO3NO2*
S 557.53±94.94 2008.89±234.98 175.05±29.50 78.12±19.83 119.61±16.50 76.61±8.57
M1 311.72±49.58 834.70±172.44 76.38±14.31 41.95±6.49 1.29±12.49 4.58±0.38
M2 223.84±36.61 566.18±88.09 44.57±8.30 31.70±8.97 12.27±6.02 4.54±1.69
ANOVA 0.0113 0.0002 0.0005 0.0738 <0.0001 <0.0001
HSD S ≥M1 ≥M2 S>M1=M2 S>M1=M2 S=M1=M2 S>M2=M1 S>M2=M1
Note: S, scallops; M1, 1-year-old mussels; M2, 2-year-old mussels. Fluxes are expressed as mg O2and µmol nutrient·kg DW–1·h–1. Sig-
nificance of analysis of variance (ANOVA) and honestly significant difference (HSD) tests comparing the influence of aquaculture
structure type (S, M1, M2) on pelagic fluxes are also given.
*%(x).
Table 3. Mean fluxes (± standard error, SE) measured at the interface of aquaculture structures standardized to 1 kg
dry weight (DW) of macrofauna (bivalve + associated fauna).
Variable Source df MS Fp
OM (%)* Zone 3 1.42 8.03 0.0012
Error 19 0.18
Biomass†Zone 3 2.91 2.77 0.0696
Error 19 1.05
Abundance‡Zone 3 3065.10 13.55 <0.0001
Error 19 226.10
*ln(x).
†ln(x+ 1).
‡%(x).
Table 4. Results of analyses of variance testing the effect of
zone (control, scallops, 1-year-old mussels, 2-year-old mussels)
on sediment organic matter content (OM, %) and macrofaunal
biomass and abundance.
Fluxes Source df MS Fp
O2Zone 3 2 471.59 1.63 0.2156
Error 19 1 515.55
NH4Zone 3 116 103 3.37 0.0401
Error 19 34 457
Si(OH)4Zone 3 133 846 12.61 <0.0001
Error 19 10 613
PO4Zone 3 2 259.01 7.84 0.0013
Error 19 288.20
NO3Zone 3 46.10 1.60 0.2220
Error 19 28.77
NO2Zone 3 17.21 7.14 0.0021
Error 19 2.41
Table 5. Results of analyses of variance testing the effect of
zone (control, scallops, 1-year-old mussels, 2-year-old mussels)
on benthic fluxes (O2, Si(OH)4, NH4,PO
4,NO
3,NO
2).
Ratio Source df MS Fp
Si/P* Zone 2 0.02 0.12 0.8879
Interface 1 38.55 276.79 < 0.0001
Zone × Interface 2 0.18 1.31 0.2850
Error 29 0.14
N/P Zone 2 130.62 3.28 0.0521
Interface 1 0.38 0.01 0.9227
Zone × Interface 2 37.84 0.95 0.3987
Error 29 39.87
*%(x).
Table 6. Results of analyses of variance testing the effects of culture
zones (scallops, 1-year-old mussels, 2-year-old mussels), interface
type (pelagic, benthic), and their interaction (Zone × Interface) on
nutrient ratios (silicate/phosphate (Si/P) and nitrogen/phosphate (N/P)).
Contribution to oxygen and nutrient pools
Oxygen consumption was observed at both interfaces (pe-
lagic and benthic) in culture zones (Fig. 4) and was a func-
tion of the interaction between zone (M1 vs. M2 vs. S) and
interface (pelagic vs. benthic; Table 7). Oxygen consumption
did not vary significantly between interfaces in M1 and M2,
but was 2.8 times greater at the benthic interface than at the
pelagic (i.e., pearl net) interface in S (Fig. 4a). Ammonium
fluxes varied significantly between interfaces in culture
zones (Table 7), such that they were twice as great at benthic
interfaces than at aquaculture structure interfaces (Fig. 4b).
Ammonium was the nutrient released in the greatest quantity
in culture zones. Silicate fluxes were a function of the inter-
action between zone and interface (Table 7) and were, over-
all, about 33 times greater at benthic than at pelagic
interfaces (Fig. 4c). Phosphate fluxes also varied between in-
terfaces (Table 7), such that benthic fluxes were more than
twice those at pelagic aquaculture structure interfaces
(Fig. 4d). Nitrate fluxes varied between interfaces and zones
(Table 7). Overall, they were almost five times greater at pe-
lagic than at benthic interfaces (Fig. 4e). As an extreme ex-
ample, the mean nitrate flux was about 22 times greater at
the pearl net interface than at the benthic interface in S
(Fig. 4e). Mean nitrate releases were greater in S and M2
than in M1. Nitrite fluxes varied significantly between zones
and interfaces (Table 7). Overall, pelagic nitrite fluxes were
twice those of benthic nitrite fluxes (Fig. 4f). Mean nitrite
releases were about five times greater in S than in M1 and
M2, which did not differ (Fig. 4f).
Discussion
Influence of mussel and scallop cultures on the pelagic
environment
The introduction of aquaculture structures in HAM in-
creased the abundance and biomass of sessile organisms in
the water column. As suggested by others (e.g., Lesser et al.
1992; Ross et al. 2004; McKindsey et al. 2006), the
aquaculture structures provided novel substrates for the set-
tlement and growth of a variety of benthic invertebrates. The
biomass and abundance of associated fauna were greater on
scallop cages and M2 lines than on M1 lines. This may be
explained by the comparatively larger surface area available
for settlement and growth on scallop cages and the greater
immersion time of M2 lines compared with M1 lines. How-
ever, the degree of biofouling on aquaculture structures ob-
served in HAM was not great relative to observations in
other shellfish culture areas around the world. Indeed, the
associated fauna only represented between 0.01% (M1) and
2.5% (M2) of the total macrofaunal biomass associated with
mussel lines in this study. In contrast, mussel socks from the
Ria de Arosa in Spain supported >400 g DW of epifauna
(34% of total biomass) for every metre of mussel sock
(Tenore and González 1976). In the Thau Lagoon (France),
the associated fauna (mainly ascidians) can represent up to
80% of total biomass on oyster ropes in July (Mazouni
1995). Likewise, the maximum DW of associated fauna per
scallop cage was 12.5 g in HAM, whereas it was almost
200 g in August in Baie des Chaleurs, eastern Canada
(Claereboudt et al. 1994).
Aquaculture structures, composed of the mooring system,
the cultivated bivalves, and the associated fauna – organic
matter complex, represent novel suspended benthic inter-
faces in the water column and may be new interfaces for
biogeochemical exchanges (Mazouni et al. 2001; Mazouni
2004; Nizzoli et al. 2006). In HAM, mussel lines and scallop
cages may be considered as suspended bivalve communities,
with associated oxygen consumption as has been observed
for benthic mussel beds by Dankers et al. (1989) and nitro-
gen and phosphate releases to the adjacent waters as has
been observed in benthic systems by Dame et al. (1984,
1985, 1989) for oyster reefs and by Asmus et al. (1995) for
mussel beds. Considering the low biomass of fauna associ-
ated with aquaculture structures in HAM, particularly in M1,
respiration and excretion by cultivated bivalves were likely
mainly responsible for the great observed pelagic fluxes, as
was noted by Richard et al. (2006) at the interface of mussel
line sections in laboratory experiments. However, cultivated
bivalves and biofouling organisms can generate considerable
amounts of organic matter (Callier et al. 2006), and this may
accumulate within aquaculture structures (Arakawa 1990;
Mazouni et al. 2001; Nizzoli et al. 2006). Thus, the observed
oxygen consumption and ammonium and phosphate releases
could also have originated from the degradation of
biodeposits trapped within the aquaculture structures, as bi-
valve biodeposits are known to be an important source of ni-
trogen (Sornin et al. 1983; Grenz et al. 1990; Mazouni et al.
1996) and phosphorus (Sornin et al. 1986; Peterson and
© 2007 NRC Canada
1498 Can. J. Fish. Aquat. Sci. Vol. 64, 2007
Fluxes Source df MS Fp
O2Zone 2 288.90 0.25 0.7836
Interface 1 8 067.29 6.87 0.0138
Zone × Interface 2 8 298.35 7.06 0.0032
Error 29 1 174.58
NH4Zone 2 14 690.10 0.52 0.5972
Interface 1 518 194.10 18.51 0.0002
Zone × Interface 2 17 969.89 0.64 0.5335
Error 29 27 988.83
SiOH4* Zone 2 0.70 2.67 0.0862
Interface 1 111.77 427.16 <0.0001
Zone × Interface 2 0.96 3.68 0.0377
Error 29 0.26
PO4* Zone 2 0.44 2.12 0.138
Interface 1 5.60 26.99 <0.0001
Zone × Interface 2 0.32 1.55 0.2302
Error 29 0.21
NO3Zone 2 126.26 4.68 0.0173
Interface 1 163.39 6.06 0.0201
Zone × Interface 2 67.21 2.49 0.1004
Error 29 26.98
NO2Zone 2 69.30 39.95 0.0010
Interface 1 23.35 13.46 <0.0001
Zone × Interface 2 4.49 2.59 0.0922
Error 29 1.73
*ln(x).
Table 7. Results of analyses of variance testing the effect of culture
zone (scallops, 1-year-old mussels, 2-year-old mussels), interface
type (pelagic, benthic), and their interaction (Zone × Interface) on
biogeochemical fluxes (O2, Si(OH)4,NH
4,PO
4,NO
3,NO
2).
Heck 1999). The increased silicate release measured at the
interface of each aquaculture structure in this study suggests
degradation of biodeposits trapped within the structures. Di-
atom cell walls contain silica embedded within an organic
matrix (Bidle and Azam 1999), and silicate releases at the
pelagic interfaces likely originate from the dissolution of di-
atom frustules (Balzer et al. 1983; Lerat et al. 1990) trapped
in biodeposits accumulated between mussel shells or in the
net of scallop cages.
Although the pelagic macrofaunal biomass in the M2 zone
was almost two (vs. M1) to five (vs. S) times greater than
that in other culture zones, of all the fluxes measured, only
pelagic oxygen consumption in M2 was greater than that ob-
served in S. In contrast with what was expected based on
biomass differences among zones, the M2 lines did not have
a greater influence on pelagic nutrient fluxes than did the
other cultures in HAM. Macrofaunal, biomass-standardized
pelagic fluxes (to 1kg PMB) were greater at the interface of
scallop cages than at the interface of mussel lines. The per-
centage of flesh DW/total DW (with shell) ranged from 14%
to 17% between bivalve species in July 2004 (M. Richard,
unpublished data), and thus size- and species-related differ-
ences in this variable cannot explain the 2–16 times greater
fluxes recorded at the interface of scallop pens. Since bi-
valve physiology depends on species (Tenore et al. 1973;
Qian et al. 2001) and individual age or size (Yukihira et al.
1998; Sukhotin and Pörtner 2000; Qian et al. 2001), 1-year-
old scallops may have greater respiration and excretion rates
per unit biomass than do 2-year-old mussels. Nevertheless,
the metabolism of 1-year-old scallops alone can probably
not entirely explain the greater nutrient releases measured at
the scallop cage interface. We suggest that the contribution
of the associated fauna – organic matter complex to pelagic
fluxes would be greater at scallop pearl net interfaces than at
mussel line interfaces because of the greater quantity of
trapped organic matter and abundance of small-sized
macrofaunal organisms (e.g., the burrowing amphipods
(Corophium sp.)) that are associated with pearl nets. Differ-
ences among aquaculture structures may also explain the
greater nitrate and nitrite releases at the interface of scallop
cages. Indeed, in contrast with mussels that are attached on
lines, scallops are held in cages. Nets of cages, as with inter-
nal and external surfaces of bivalves (Welsh and Castadelli
2004), may be colonised by nitrifying bacteria. The dis-
solved products excreted by scallops, such as ammonium,
could diffuse through the net of the cages, stimulate the ni-
trification process, and be released as nitrite and nitrate
forms to the adjacent water. In contrast, ammonium excreted
by mussels was released directly into the adjacent water.
Moreover, the water exchanges through the mesh of scallop
cages, and the bioturbation activities (burrow construction
and irrigation) by dense amphipod (Corophium sp.) popula-
tions may favour the oxygenation and degradation of the
trapped organic matter (Pelegri and Blackburn 1994;
Mermillond-Blondin et al. 2004; 2005), stimulate the nitrifi-
cation process (Henricksen and Kemp 1988; Gilbert et al.
1997; Christensen et al. 2003), and enhance oxygen and nu-
trient fluxes (Mermillond-Blondin et al. 2004; 2005) at scal-
lop cage interfaces.
Influence of mussel and scallop cultures on the benthic
environment
Dense assemblages of filter-feeding bivalves remove sus-
pended matter from the water column and transfer it as feces
and pseudofeces to the bottom (Peterson and Heck 1999;
Cranford et al. 2003). Indeed, shellfish farms are well known
to enhance sedimentation rates due to bivalve biodeposition
(Dahlbäck and Gunnarson 1981; Hatcher et al. 1994; Callier
et al. 2006). In HAM, the organic matter content in the first
2 cm of sediment beneath suspended mussel lines was more
than twice that observed in the control zone. This organic
matter enrichment may originate from the accumulation of
© 2007 NRC Canada
Richard et al. 1499
Fig. 3. Mean (±standard error) pelagic macrofaunal (a,b) biomass and (c) abundance in scallop (S), 1-year-old mussel (M1), and
2-year-old mussel (M2) zones in Havre-aux-Maisons Lagoon. Solid bars represent the biomass or abundance of the cultivated bivalves,
whereas hatched bars represent biomass and abundance of the associated fauna. Note that (b) focuses on the mean biomass of associ-
ated fauna among culture zones and that the scale of the yaxis differs from that in (a). Different letters indicate significant (p< 0.05)
differences among culture zones.
mussel feces and pseudofeces on the bottom, as observed by
several authors (Dahlbäck and Gunnarsson 1981; Stenton-
Dozey et al. 2001; Hartstein and Rowden 2004). In contrast,
scallop cages did not induce significant organic enrichment
in the first 2 cm of sediment. This may be explained by the
low macrofaunal biomass (bivalves plus associated fauna) in
scallop cages as compared with that associated with mussel
lines. Mallet et al. (2006) found a similar result for oyster
culture in New Brunswick (Canada). Alternatively, the great
variability of sediment OM in the control zone could have
masked the influence of scallop cages on sediment organic
enrichment.
In contrast with other shellfish cultures (see Hatcher et al.
1994; Grant et al. 1995; Christensen et al. 2003), the sus-
pended bivalve cultures in HAM did not substantially mod-
ify the benthic macrofaunal biomass in culture zones.
However, great variability of benthic biomass in the control
zone may have masked the effect of mussel culture. Indeed,
benthic biomass tended to be lowest at mussel sites. In-
creasing the number of replicates to decrease uncertainty as-
sociated with treatment means would allow this hypothesis
to be better evaluated. The benthic macrofaunal abundance
was six times lower in mussel cultures than in the control
zone. This change is likely due to the organic enrichment
observed under mussel lines, as has been noted in several
studies (e.g., Mattsson and Lindén 1983; Hartstein and
Rowden 2004).
High sediment OM is known to stimulate microbial
(Dahlbäck and Gunnarson 1981; La Rosa et al. 2001) and
macrofaunal (Pearson and Rosenberg 1978) activity and
consequently increase oxygen consumption (Mattsson and
Lindén 1983; Christensen et al. 2003; Cranford et al. 2003).
Indeed, oxygen consumption measured under aquaculture
structures is often greater than that measured outside the
farms (Hargrave et al. 1993; Mazouni et al. 1996;
Christensen et al. 2003). In HAM, although sediment or-
ganic enrichment and decreased macrofaunal abundance was
observed under suspended mussel lines, oxygen consump-
tion did not differ between the control and culture zones.
This was also observed by Stenton-Dozey et al. (2001) in
South Africa, Grant et al. (1995) in Nova Scotia (eastern
Canada), and Richard et al. (2007) in Grande-Entrée La-
goon. Benthic oxygen consumption is driven by the respira-
tion of organisms and by the microbial-mediated oxidation
of organic matter and reduced inorganic metabolites (Nickell
et al. 2003). Since respiration of the macrofaunal community
depends partly on biomass (Mazouni et al. 1996) and abun-
dance (Nickell et al. 2003), the benthic oxygen demand ob-
© 2007 NRC Canada
1500 Can. J. Fish. Aquat. Sci. Vol. 64, 2007
Fig. 4. Mean (±standard error) pelagic and benthic fluxes measured in scallop (S), 1-year-old mussel (M1), 2-year-old mussel (M2),
and control (C: only for benthic fluxes) zones in Havre-aux-Maisons Lagoon: (a) oxygen consumption (O2) and (b) ammonium (NH4),
(c) silicate (Si(OH)4), and (d) phosphate (PO4) fluxes. Different letters indicate significant (p< 0.05) differences among culture zones
for a given interface (i.e., benthic or pelagic). Asterisks (*) indicate a significant difference between interface types for a given culture
zone (i.e., S, M1, or M2).
served in mussel cultures and control zones are likely driven
by different processes. The measurement of CO2production
and calculation of benthic respiratory quotient (CO2/O2)in
dark conditions would have permitted to distinguish aerobic
and anaerobic processes that drove oxygen demand in each
experimental zone (Hargrave and Phillips 1981; Hatcher et
al. 1994; Welsh 2003).
Benthic ammonium, phosphate, and silicate fluxes were
two–five times greater in bivalve culture than in control
zones. The large ammonium and phosphate releases mea-
sured at the benthic interface in culture zones could result
from the degradation of bivalve feces and pseudofeces, as bi-
valve biodeposits are rich in nitrogen and phosphorus
(Kautsky and Evans 1987). Similar to what may occur for
the suspended interface, higher silicate fluxes under
aquaculture structures could originate from the dissolution
of diatom tests trapped in biodeposits accumulated at the
benthic interface (Balzer et al. 1983). Drastic increases in
nutrient fluxes are often correlated with biodeposit accumu-
lation on the bottom under shellfish farms (Baudinet et al.
1990; Grenz et al. 1992; Christensen et al. 2003). Since scal-
lop cages did not induce organic enrichment in the underly-
ing sediments, great benthic nutrient fluxes in the zone could
signify that scallop biodeposits reaching the water–sediment
interface beneath the cages were completely remineralized
and did not accumulate.
The influence of mussel lines on sediment organic content
and macrofauna communities was greater than that of scal-
lop cages. Nevertheless, in contrast with what was expected,
nutrient fluxes were not significantly greater in M2 than in
M1 and S zones. The quantity and quality of biodeposits un-
derneath aquaculture structures could vary among culture
zones, as biodeposition rate and biodeposit composition vary
according to bivalve species (Shumway et al. 1985) and age
(Callier et al. 2006). Great nitrite releases in S may result
from nitrification processes enhanced by bioturbation by the
dense subsurface deposit feeder population (Pectinaria sp.)
observed in that zone. Nitrification is favoured (Jenkins and
Kemp 1984; Kristensen and Blackburn 1987) by a deeper
oxic layer and increased oxygen diffusion through finer sedi-
ments due to bioturbation (Pearson and Rosenberg 1978).
Pelagic vs. benthic interfaces: relative contributions and
roles
Several authors (e.g., Kaspar et al. 1985; Baudinet et al.
1990; Mazouni et al. 1996) have suggested that nutrient re-
generation in shallow waters is ensured by benthic
remineralization, as sediments may regulate the production
(fluxes) and standing stocks (concentrations) of nutrients in
the water. This study showed that mussel lines and scallop
cages acted as additional sinks for oxygen and sources of
nutrients in the water column in HAM. Thus, both pelagic
and benthic interfaces contribute to the production and
standing stocks of nutrients and oxygen in the water column.
This study highlighted that the contribution of aquaculture
structures to oxygen and nutrient pools was considerable
when compared with benthic interfaces. Indeed, the contri-
bution of mussel lines (vs. benthic interface) to oxygen
pools was approximately 50% of the total combined con-
sumption in the mussel zones, whereas scallop cages ac-
counted for approximately 25% of the total oxygen
consumption in the scallop zone. The contributions of
aquaculture structures to the total ammonium and phosphate
releases by both interfaces were greater than 30%. Only two
other studies have addressed this issue: one for oyster
(Mazouni 2004) and the other for mussel (Nizzoli et al.
2006) culture. In contrast with the current study, the contri-
bution of mussel ropes to the ammonium pool in Sacca di
Goro Lagoon, Italy, was similar to that of the benthic inter-
face (1200 µmol·m–2·h–1; Nizzoli et al. 2006). In Thau La-
goon, the contribution of oyster ropes to the total ammonium
produced by both interfaces was greater than 90% in July
(3000 vs. 250 µmol·m–2·h–1 for sediment; Mazouni 2004).
The greater ammonium releases and contributions to ammo-
nium standing stocks in Italy and France likely result from
the greater cultivated bivalve biomasses in those locations
relative to that cultured in HAM. Indeed, biomass of mussels
in Sacca di Goro in July (3 kg wet weight·m–2; Nizzoli et al.
2006) was more than two times greater than the biomass of
M2 in HAM (460.78 g DW·m–2 with shell = 1.25 kg wet
weight·m–2 in this study), and the oyster biomass in Thau
Lagoon (Mazouni 2004) was more than 15 times greater
(1000 vs. 68.51 g AFDW·m–2). One possible effect of nutri-
ent releases at aquaculture structure interfaces could be an
enhancement of primary production through a feedback loop
© 2007 NRC Canada
Richard et al. 1501
Fig. 5. Mean (±standard error) sediment organic matter (OM, %)
content (a), benthic macrofaunal biomass (b), and abundance
(c) measured in control (C), scallop (S), 1-year-old mussel (M1),
and 2-year-old mussel (M2) zones in Havre-aux-Maisons Lagoon.
Different letters indicate significant differences among culture zones.
(phytoplankton consumed by the bivalves would be rapidly
remineralized), as suggested by Dame et al. (1985) and
Dame and Libes (1993) for oyster reefs and by Kaspar et al.
(1985) for mussel farms. This aspect is enhanced in closed
system such as the Thau Lagoon, where the water residence
time is 220 days (Bacher et al. 2005), relative to that in to
more open systems such as HAM lagoon, where the water
mass is renewed more rapidly (20–35 days; Koutitonsky and
Tita 2006).
Biogeochemical processes differ between pelagic and ben-
thic interfaces, as shown by the mean Si/N/P ratios (13-fold
difference for silicates). In HAM, silicate releases at benthic
interfaces were >30 times those at aquaculture structure in-
terfaces. This result highlights the dominant role of benthic
relative to pelagic interfaces for silicate cycling, with a turn-
over known to be faster because of bivalve biodeposition
(Ragueneau et al. 2002; Thouzeau et al. 2007). Disequilibria
in nutrient release kinetics can alter nutrient ratios and the
specific composition of phytoplankton communities
(Baudinet et al. 1990). The two interfaces could therefore
have a different influence on phytoplankton production and
composition. The great silicate supply by the benthic inter-
face may favour siliceous phytoplankton production (Egge
and Asknes 1992), whereas the great pelagic nitrogen re-
leases may favour nonsiliceous phytoplankton (Officer et al.
1982; Smayda 1990). Pelagic nitrogen was mainly released
as ammonium, which may favour the growth of small-sized
phytoplankton (Officer et al. 1982). Aquaculture structures
also play a role in nitrate and nitrite cycling in HAM, as they
may enhance the standing stocks of these nutrients. The pro-
portional contribution of pelagic releases to nitrate and ni-
trite pools varied between 65% and 95% (of the combined
total released by benthic and pelagic interfaces). Nitrite–
nitrate availability was greater in S than in M1 and M2,
which may favour the production of large-sized phyto-
plankton (Officer et al. 1982).
This study had three main findings. (i) Mussel lines and
scallop cages acted as suspended macrofaunal communities
that increased oxygen consumption and nutrient releases (es-
pecially ammonium and phosphate) in the water column.
(ii) Mussel culture induced organic matter enrichment in the
sediment and decreased benthic macrofaunal abundance, in
contrast with scallop culture, which did not. Nevertheless,
great nutrient releases were observed at the water–sediment
interface in all zones with suspended bivalve culture. This
study is the first to show that the influence of suspended
scallop cages on biogeochemical fluxes could be similar to
the well-documented influence of suspended mussel culture.
(iii) Pelagic interfaces also contribute to oxygen and nutrient
fluxes. Their contribution in HAM is slight compared with
two more productive European bivalve farms. Pelagic and
benthic interfaces had different influences on nutrient cycles;
benthic interfaces exhibited major silicate turnover, whereas
aquaculture structures (especially scallop cages) mainly
modified nitrate and nitrite pools. This study emphasized
that the influence of suspended aquaculture structures on
biogeochemical cycles should not be ignored, even if the
density of cultivated bivalves is low as is the case in the Îles-
de-la-Madeleine. A better understanding of the seasonal
trends for these measures should be the next step to integrate
carrying capacity models for the development of sustainable
aquaculture. In contrast with what was expected, M2 lines did
not have a greater influence on pelagic and benthic fluxes
than did other culture types. Future manipulative experiments
could test (i) the influence of the species being cultivated, of
individual age–size and bivalve density–biomass, and of the
associated fauna – organic matter complex on pelagic fluxes;
and (ii) the influence of species-related biodeposition gradi-
ents on sediment organic matter enrichment, benthic nutrient
fluxes, and benthic community changes.
Acknowledgements
The authors thank J. Clavier for precious advice during ben-
thic chamber construction; P. Robichaud and B. Chenard for
their help on the waterproof systems; and Y. Samson,
S. Chartrand, and J.S. Ouellet for help with electronics. The au-
thors show gratitude to Fisheries and Oceans Canada (Mont-Joli)
for boat facilities and to M. Fournier, A. Huet, and S. Vigneau,
who provided the mussel lines and scallop cages. Thanks go to
the BECCS team (Bivalve Environmental Carrying Capacity
Studies: M. Callier, F. Hartog, M. Leonard, L. Solomon) and to
A. Dubost and W. Dubost for their precious help in the field.
The authors thank B. Myrand and G. Tita for providing facilities
in the Îles-de-la-Madeleine and S. Roy and A. Trottet for the
loan of a fluorometer. L. MacLaughlin performed the nutrient
analyses on A. Gagné’s equipment, while M. Fréchette, L. Gi-
rard, P. Goudreau, and R. Larocque provided furnaces. Thanks
also go to B. Hargrave, B. Sundby, J. Clavier, and G. Boucher
for commenting on an earlier version of this paper. This study
was funded by an Aquaculture Collaborative Research and
Development Program (ACRDP) from Fisheries and Oceans
Canada, ISMER, RAQ (Réseau Aquaculture Québec), and by
SODIM (Société de développement de l’industrie maricole) to
P. Archambault and C.W. McKindsey.
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