ICES CM 2008/H:15
Theme H: Ecological Carrying Capacity in shellfish Culture
Not to be cited without prior reference to the author
Secondary productivity of fish and macroinvertebrates in mussel aquaculture sites
Philippe Archambault1*, Brianna G. Clynick1,2, Christopher W. McKindsey2,1
1.
Institut des sciences de la mer (ISMER), Université du Québec à Rimouski, 310, allée des Ursulines,
CP 3300, Rimouski (Québec) Canada G5L 3A1
2. Fisheries and Oceans Canada, Maurice Lamontagne Institute, Environmental Sciences Division, 850 route de
la mer, P.O. Box 1000, Mont Joli, Quebec, Canada, G5H 3Z4
Artificial reefs provide shelter for many species and aquaculture structures may function in a
similar way in that they provide a complex three-dimensional habitat for marine organisms and/or
modify the surrounding environment. Furthermore, aquaculture structures may increase the
productivity of mobile species similarly to natural complex habitats, such as seagrass beds. This
project tested the general hypothesis that suspended bivalve culture increases the abundance and
productivity of fish and macroinvertebrates. Fish and macroinvertebrates were sampled in
different areas within farms sites and in adjacent natural vegetated and unvegetated habitats in the
Magdalen Islands, eastern Canada. The results demonstrated that fish and macroinvertebrate
assemblages are not similar between mussel sites and natural structurally complex seagrass beds.
Winter flounder and rock crab were abundant in mussel farms. As future development of mussel
aquaculture increases in many regions around the world, the methods presented here will provide
baseline information on the abundance of fish and macroinvertebrates associated with
aquaculture sites.
Keywords: mussel aquaculture, secondary productivity; environmental impact; benthic
macroinvertebrates and fish
*Contact author: tel: +1 (418) 723-1986 ext 1765, fax: +1 (418) 724-1842, email: [email protected]
INTRODUCTION
Aquaculture production of fish and
shellfish has expanded over the past decade,
leading to increasing concerns about
environmental consequences. Consequently,
extensive research has documented the
environmental impacts of aquaculture farms in
coastal waters. The majority of this research
has investigated the benthic environment
under and near to farms as it relates to the
input of organic matter into the ecosystem
(Callier et al., 2006; Cranford et al., 2007;
Hargrave et al. 2008). Impacts of aquaculture
on the surrounding environment have been
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ICES CM 2008/H:15
Theme H: Ecological Carrying Capacity in shellfish Culture
generally classified as “negative” and are
related to issues concerning water quality,
sediment accumulation beneath farms, benthic
enrichment and effect on adjacent habitats
(Delagado et al., 1999; Crawford, 2003). In
contrast, little research has investigated
aquaculture sites as novel habitats that may
alter the abundance and productivity of
organisms (Laffaille et al., 2001; Dempster et
al., 2002; D’Amours et al., 2008).
Aquaculture farms provide extensive
3D-structures and therefore may also provide
habitat for marine organisms that live in a
given area. Previous work that has
investigated assemblages of wild fish around
fish farms have found large differences in the
composition and abundance of fish associated
with farm sites compared with nearby control
sites (Carrs, 1990; Dempster, 2002). These
artificial structures increase the structural
complexity of sandy bottoms in a way liken to
natural structurally complex habitats such as
seagrass beds and rocky reefs and could
influence abundance and diversity of
organisms.
The potential impacts of the
installation of mussel farms in coastal areas
have generally not been considered, as unlike
other types of aquaculture they are perceived
as a benign use of coastal waters as they do
not require the addition of food (Inglis and
Gust, 2003; Crawford et al., 2003). Their
effects on the surrounding environment
however are relatively unknown. For example,
the concentration of artificially large densities
of shellfish may be a food source for many
predators including fish, macroinvertebrates,
such seastars (Inglis and Gust, 2003) and
ducks (Larsen & Guillemette 2000). Likewise,
the extensive hard substrata of rope and
mussels may favour the establishment of
epiphytic algae and sessile invertebrates that
are also consumed by higher trophic levels
(Morrisey et al., 2006). McKindsey et al
(2006) discussed all these effects in more
details.
The aim of this study was to determine
interactions between bivalve aquaculture and
the abundance and diversity of macrobenthic
invertebrates and fishes. More specifically, we
tested the hypothesis that the abundance of
benthic fish and macroinvertebrates would be
greater in bivalve farms (an artificial
structurally complex habitat) than areas of
unvegetated sand substrata and comparable to
those associated with seagrass beds (natural
structurally complex habitat).
METHODS
Two farm sites were selected for this
study, one in the Great-Entry Lagoon (GEL)
and one in Hâvre aux Maisons (HAM) in the
Magdalen Islands, eastern Canada (Fig. 1).
Mussels (Mytilus edulis) are cultured on
longlines and reach commercial size after 2year. In GEL, the mussel site covers an area of
approximately 2.5 km2, where as in HAM the
farm surface area is 1.25 km2. In both lagoons,
the farm sites are divided into two distinct
zones with 0+ mussels and 1+ mussels (Fig.
1). The 1+ mussels are replaced by juveniles
each fall following harvesting. Longlines are
separated by 20 m and 12 m at GEL and HAM
respectively with and average depth between
5-7 m.
Field sampling methods
Sampling was carried out in June,
August and November 2004 over a period of
one
week
each
time.
Fish
and
macroinvertebrate assemblages were sampled
in four types of habitat in each lagoon;
unvegetated sandy substrates under mussel
lines with 0+ mussels, unvegetated sandy
substrates under mussel lines with 1+ mussels,
unvegetated sand substrates away from mussel
lines and Zostera beds. Five sites were
randomly selected in each habitat at each time,
except for 1+ mussels in GEL where only
three sites were selected in June and August
due to the small size of this section of the
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ICES CM 2008/H:15
Theme H: Ecological Carrying Capacity in shellfish Culture
ure
farm. 1+ mussel sites were not sampled in
November because harvesting had occurred.
Sites were separated by 100s of metres to
several kms.
Fig. 1. Location of the mussel farms (polygons)
in Great-Entry Lagoon (GEL) and Hâvre aux
Maisons (HAM) in the Magdalen Islands,
Canada.
The
abundance
of
fish
and
macroinvertebrates was measured using two
methods. The abundance was used as a proxy
for secondary productivity. First, 2 to 5 trawls
(small beam trawl 1 m aperture) was used to
sample benthic organisms at each site. In the
mussel sites, trawls were done parallel to the
mussel structures. The length of each trawl
varied due to space and time constraints, thus,
all data was standardised to a trawl length of
100 m. Second, a single crab trap was
deployed at each site (between 1 and 3 hours).
Each catch was expressed as number of crabs
per hour to standardise data. No significant
effect on the catch rate of crabs (r2 = 0.006, P
> 0.05) was observed among mooring time of
the traps.
differences among habitats within times, not
for differences among times. Furthermore,
lagoons were analysed separately because 1+
mussels in GEL were not sampled in
November. Frequencies of occurrence were
also examined for each species across the
different habitats.
Differences in fish assemblages among
habitats were tested using non-parametric
multivariate techniques using Bray-Curtis
measures of dissimilarity (Bray and Curtis,
1957) calculated from untransformed data.
Two-way nested analyses of similarities
(ANOSIM) tested for differences in the
composition of assemblages among habitats,
with sites nested within habitats (Clarke and
Green, 1988). Non–metric multidimensional
scaling (nMDS) plots were used to illustrate
spatial patterns of assemblages of fish in
different habitats (Clarke, 1993). SIMPER
analysis (Clarke, 1993) was used to determine
the taxa most responsible for any significant
differences detected among assemblages.
RESULTS
Sampling revealed a small suite of
species present in all habitats in both lagoons,
including eight species of fish and three
species of macroinvertebrates. The winter
flounder, Pseudopleuronectes americanus,
was the most commonly occurring species in
mussel and unvegetated sites. The four spined
stickleback, Apltes quadracus, was the most
common species in seagrass sites. The sand
shrimp, Crangon septemspinosa, was common
to all habitats (Table 1). Most other species
were relatively patchy in their occurrence.
Statistical methods
Analysis of variance (ANOVA) was
used to test differences in the total number and
types of fish and macroinvertebrates and the
abundance of common species among habitats.
Student-Newman-Keuls tests (SNK) were
used to compare significant source of
variation. Each time was analysed separately
because hypotheses were aimed to identify
Abundance,
assemblages
diversity
and
composition
The number of species was very low
across all habitats. However, on many
occasions, the number of species associated
with Zostera beds was greater than all other
habitats (Fig. 2a). This pattern was significant
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ure
in August in both lagoons (F = 4.78, P <
0.01). In contrast, the total abundance of fish
and invertebrates was similar in the three
habitats (Fig. 2b). There was an exception in
August, when the total abundance of fish and
macroinvertebrates was significantly greater in
Zostera beds (F = 40.43; P < 0.001). The great
abundance of stickleback present in Zostera
bed at this time could explain this result.
Winter flounder was found in similar
abundances in both types of mussel sites and
unvegetated sites (Fig. 2c), whereas it was
only present in Zostera beds in very low
abundance in both lagoons across all sampling
times. This difference between the habitats
was significant in June (F = 9.74, P < 0.001)
and August (F = 6.38, P < 0.01). In contrast,
the four-spined stickleback was significantly
more abundant in Zostera beds than the other
three habitats (F = 15.81, 39.73, 8.89, 8.33, for
June and August in both lagoons and
November in GEL and HAM respectively, P <
0.001). The four-spined stickleback was often
absent entirely in the mussel and sand habitat
(Fig. 2d). All other fish species were present in
low numbers (Table 1).
The
three
species
of
macroinvertebrates - the rock crab, Cancer
irroratus, the American lobster, Homarus
americanus and the sand shrimp, C.
septemspinosa - did not showed any consistent
patterns among the four types of habitat. A
great variability was observed between the two
lagoons and across the three sampling times
(Fig. 2e & f).
The effects of habitat on invertebrate
and fish assemblages were consistent in both
lagoons and across all sampling times. The
results of the ANOSIM (Table 2) and the
nMDS showed that there were significant
differences
between
the
assemblages
associated with seagrass beds and those
associated with mussel sites and unvegetated
sites in both lagoons across all sampling times.
Fig. 2. Mean (+SE) (a) number of species; (b)
number of individuals and (c–f) abundance of
common species at M1 (grey), M2 (black), Sand
(white) and Zostera (hatched) in GEL and HAM
at the three sampling dates.
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Theme H: Ecological Carrying Capacity in shellfish Culture
Table 1. List of taxa recorded and their frequency of occurrence (% transects present) at sites with 0+ mussels (M1); 1+ mussels (M2);
sand and Zostera across the three sampling times.
Family
Pleuronectidae
Gasterosteidae
Labridae
Pholidae
Cottidae
Phycidae
Bothidae
Gadidae
Clupeidae
Nephropidae
Cancridae
Crangonidae
Species
Pseudopleuronectes americanus
Apeltes quadracus
Tautogolabrus adspersus
Pholis gunnellus
Myoxocephalus octodecemspinosus
Urophycis tenuis
Scophthalmus aquosus
Microgadus tomcod
Clupea harengus
Homarus americanus
Cancer irroratus
Crangon septemspinosa
Common name
Winter flounder
Four spine stickleback
Cunner
Rock gunnel
Longhorn sculpin
White hack
Windowpane
Atlantic tomcod
Atlantic herring
American lobster
Rock crab
Sand shrimp
M1
69
6
4
7
3
0
0
0
0
6
0
58
M2
81
15
0
11
4
0
1
0
0
4
0
64
Table 2. R – values (ANOSIM) for comparisons of assemblages in the four habitats (M1, M2, S &
Z) at the two locations (GEL & HAM) at the three sampling dates. * = P < 0.05, ** = P < 0.01.
(i) Global R values
GEL
June
0.407**
August
0.626**
November
0.554**
(ii) Pairwise comparisons
M1
June
M2
0.12**
S
0.17**
Z
0.88**
August
M2
0.1788
S
0.18*8
Z
1.00**
November
M2
S
0.028
Z
0.99*
HAM
0.578**
0.666**
0.548**
M2
0.04*
0.85*
0.068
1.00*
-
S
M1
M2
S
0.78**
0.02**
0.18**
1.00**
0.23**
1.00**
0.69**
0.84**
0.2488
0.0688
0.98**
0.1688
1.00**
1.00**
0.99*
0.118
0.278
1.00*
0.218
1.00*
1.00*
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Sand
65
27
13
11
4
0
0
0
0
12
0
59
Zostera
22
88
20
8
6
3
0
1
5
18
0
63
ICES CM 2008/H:15
Theme H: Ecological Carrying Capacity in shellfish Culture
SIMPER analysis indicated that
winter flounder and four-spine stickleback
accounted for the majority of the
dissimilarity between Zostera beds and the
other habitats (70 to 97% contribution).
Fig. 3. nMDS plots on the assemblages of fish
and macroinvertebrates in the four habitats (▲=
M1, ▼= M2, ■ = Sand, ● = Zostera) at the two
lagoons (GEL, black symbols; HAM empty
symbols) in (a) June, (b) August and (c)
September.
DISCUSSION
The results of our study highlighted
large differences in the assemblages of fish
and macroinvertebrates associated with
mussel farms to those associated with
seagrass beds. Differences in assemblages
were almost entirely driven by the two most
dominant species present; winter flounder
and the four-spine stickleback. Winter
flounders are habitat generalists, occurring
on shallow substrates across a range of
sediment types and in both vegetated and
unvegetated areas (Sogard and Able, 1991).
In some instances, they have been found to
be more abundant in unvegetated areas than
seagrass beds (Sogard, 1992). In contrast,
Smith et al. (2008) observed more fish in
seagrass than over sand in the temperate
waters of Victoria in Australia. Sticklebacks
are commonly associated with aquatic
vegetation, both benthic and floating (Scott
and Crossman, 1973). Naturally complex
habitats, such as seagrass beds, generally
support a greater abundance and diversity of
fish and invertebrates than do nearby
unvegetated sandy substrates. It is suggested
that the presence of vegetation and
associated epibiota add an extra trophic
resource to the base of the food web and
increase organism production through
enhanced food availability (Lubbers et al.,
1990). Therefore, Zostera beds may offer
protection from predation that mussel farms
do not for this species. Several other species
of fish, including the white hake, U. tenuis,
and Atlantic herring, C. harengus, were also
almost exclusively found in seagrass beds,
which suggests that these species also have
specific habitat requirements that seagrass
beds provide and that cannot be mimicked
by other coastal structures. However, our
results did not support the fact that Zostera
beds have systematically more fish and
macroinvertebrate species than mussel sites
and the differences in abundance was mainly
due to one species of fish, the four-spine
stickleback .
No differences were found in
assemblages and diversity of fish and mobile
macroinvertebrates associated with mussel
farms to those in surrounding unvegetated
sandy sites. Our results differ greatly to
those of other authors who have reported
considerably larger abundance and number
of species of fish at fish farming sites
compared to nearby sandy bottoms with no
overlying aquaculture structures (Dempster
et al., 2002; Boyra et al., 2004). This
difference may be largely due to the low
diversity in the lagoons studied, as the
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Theme H: Ecological Carrying Capacity in shellfish Culture
composition of fish assemblages in mussel
farms likely depends on the available pool of
species in the area (Morrisey et al., 2006). A
second possibility that could explain the lack
of differences between mussel and sandy
areas is the sampling techniques used in this
study. The majority of previous work has
measured the distribution of pelagic species
around fish and mussel farms using scuba
surveys (e.g. Dempster et al., 2002; Boyra et
al., 2004). In this study, we only measured
the distribution of benthic species in the near
vicinity of mussel lines, not directly under
them, as trawling was done between and
parallel to mussel lines. Previous studies
have shown that the attraction of fish to new
structure is very localised with numbers
directly adjacent or under structures being
much greater than numbers in open water as
little as 2 metres away (Clynick, unpublished
data). Additionally, similar work using scuba
surveys to evaluate the abundance of fish
and macroinvertebrates in Prince Edward
Island (ca. 100 km southwest of the
Magdalen Islands) (D’Amours et al. 2008)
and in the Magdalen islands (Clynick,
unpublished data) showed that many fish
and macroinvertebrates are found directly
under the mussel lines and at close proximity
to anchor blocks. Such small-scale
distribution of macroinvertebrates has also
been observed in New Zealand where sea
stars aggregate directly under mussel lines,
feeding on fallen mussels (Inglis and Gust,
2003).
Our results suggest that aquaculture
does not appear to be having a negative
impact on the abundance of associated
benthic fish and macroinvertebrates. For
example, flatfish may be sensitive to
pollution because they reside in bottom
sediments where chemical contaminants
accumulate (Johnson et al., 1998).
Therefore, if mussel farms are a potential
source of pollution it is likely that this
species might be absent below and around
culture sites. We found no difference,
however, in the abundance winter flounder
under mussel lines to areas away from farms
but this commercial species was less
abundant in the Zostera beds.
The ecological implications of
deploying artificial structures, including
aquaculture structures, in lagoons, bays or
estuaries may be dependent on where these
structures are built and the natural habitats
that are most affected (Bulleri, 2005).
Mussel longlines are built over sand and are
therefore supplementing soft sediment with
hard substrata. In such instances, it is
generally not possible to preserve the natural
patterns of organisms, but it may be possible
to minimise changes to patterns of
distribution and productivity of organisms.
In this study, we reported no difference in
the abundance and diversity of benthic fish
and macroinvertebrates associated with
mussel farms to those in adjacent natural
unvegetated habitats. However, we observed
large differences in assemblages between
mussel farms and Zostera beds, which
suggests that artificial habitats may not be
analogous to natural structurally complex
habitats.
This study is important as mussel
aquaculture develops in many regions
around the world, the results and techniques
developed in this study will provide baseline
information of the abundance and eventually
productivity of fish and macroinvertebrates
associated with aquaculture sites. The next
step of this study will be to evaluate the
productivity with biochemical techniques
such as nucleic acid analyses. Nucleic acid
measurements can provide a proxy for
growth as the concentration of RNA per cell
varies in proportion to protein synthesis and
growth while the DNA concentration of each
cell remains relatively constant (Buckley et
al.,
1999).
Previous
studies
have
documented strong relationships between
RNA concentrations and RNA/DNA ratios
and instantaneous growth rates for many
species, including winter flounder (Kurpat et
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ICES CM 2008/H:15
Theme H: Ecological Carrying Capacity in shellfish Culture
al., 2002). This information and our results
are essential if logical conclusions on the
impact of aquaculture on the ecosystem are
to be made.
Callier MD, Weise AM, McKindsey CW,
Desrosiers G, 2006. Sedimentation rates in a
suspended mussel farm (Great-Entry
Lagoon, Canada): biodeposit production and
dispersion. Mar. Ecol. Prog. Ser. 322:129141.
ACKNOWLEDGEMENTS
Carss DN, 1990. Concentrations of wild and
escaped fishes immediately adjacent to fish
farm cages. Aquaculture 90 :29-40.
Special thank P. Robichaud, A. Weise,
M. Callier, F. Hartog, M. Leonard, and L.
Solomon for their precious help in the field.
Authors show gratitude to Fisheries and
Oceans Canada (Mont-Joli) for boat
facilities. This study was funded by an
Aquanet Canada (Network of Centres of
Excellence Program) and a (Réseau
Aquaculture Québec) to PA and CM. BC
was supported by a FQRNT (Fonds
Québécois de la Recherche sur la nature et
les technologies) postdoc fellowship.
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