Environmental Pollution 316 (2023) 120614

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Shellfish as a bioremediation tool: A review and meta-analysis

Giulia Filippini a, *, Katherine A. Dafforn a, b, Ana B. Bugnot c, d
a
School of Natural Sciences, Macquarie University, North Ryde, NSW, 2109, Australia
b
Sydney Institute of Marine Science, Mosman, NSW, 2088, Australia
c
School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia
d
Commonwealth Scientific and Industrial Research Organisation, Brisbane, QLD, 4001, Australia

A R T I C L E I N F O A B S T R A C T

Keywords: Over the last century, human activities have increased the amount of nutrients inputs to terrestrial and aquatic
Bioremediation ecosystems. These activities have altered nitrogen (N) and phosphorus (P) cycling, causing substantial changes in
Meta-analysis ecosystem function such as provision of clean air and water. Strategies that reduce and remove excess nutrients
Shellfish
are urgently needed to remediate impacted systems. Reef-forming shellfish (oysters and mussels) can play a
Nutrient fluxes
Denitrification
crucial role in nutrient cycling, particularly in N removal from aquatic systems by providing substrate for mi­
Environmental factors crobial colonisation and enhancing microbial denitrification in the surrounding sediments. However, the po­
tential for shellfish to enhance nutrient cycling (and denitrification) will likely vary spatially and in response to
several environmental factors. Here, we used 1) a qualitative analysis to review nutrient processes occurring on
shellfish; and 2) a meta-analysis to evaluate the influence of shellfish on benthic metabolism and nutrient cycling
in surrounding sediments, and how that is influenced by environmental factors such as grain size, seasonality,
water body type, and tidal position. Overall, we found that shellfish increased oxygen consumption, with
3-
consequent release of ammonia (NH+ 4 ) and phosphate (PO4 ) from shellfish and their surrounding sediments.
These parameters did not depend on grain size, water body type and tidal height, but the release of PO3- 4 was
variable between seasons, being highest during summer and autumn. Shellfish presence also enhanced denitri­
fication measured as dinitrogen gas (N2) efflux on both reefs and sediments. Denitrification was highest in la­
goons; in sandy sediments; and during the warmest season (summer). Thus, our findings highlight that
environmental context can mediate the effects of shellfish reefs on sediment function. This information is
important for managers seeking to use these animals as an effective bioremediation tool.

1. Introduction remineralisation of nutrients worldwide due to processes occurring in

Bioavailable nitrogen (N) and phosphorus (P) are limiting resources
in natural ecosystems; hence they control primary productivity and
underpin the biodiversity and function of ecosystems on Earth. How­
ever, over the last century, human activities have increased the amount
of these bioavailable nutrients in terrestrial and aquatic systems through
deforestation, burning of fossil fuels, the use of fertilisers and organic
waste. These activities have altered N and P cycling at global scales,
causing substantial changes in ecosystem function (Steffen et al., 2015;
Vitousek et al., 1997). For example, increased emissions of nitrous oxide
and nitric oxide into the atmosphere have contributed to global warm­
ing, formation of photochemical smog and production of acid rain
(Gruber and Galloway, 2008).
Coastal marine ecosystems are responsible for 50% of the
the widely distributed soft-sediment habitats (Middelburg et al., 1997;
Nixon, 1981). In addition, biogenic habitats such as mangroves, salt­
marsh, seagrass, and shellfish reefs also play key roles in the processing
of nutrients in these systems (Fourqurean et al., 2012; Kellogg et al.,
2014; Smyth et al., 2016; Valiela and Cole, 2002). Notwithstanding their
importance to the health of global ecosystems, these coastal systems are
often highly degraded due to eutrophication from excess nutrients in­
puts derived from fertilizers, urban sewage, industrial wastewater, and
agricultural runoff, which accumulate in sediments (Herbert, 1999;
Lehtoranta et al., 2009). Increased bioavailable N and P in these systems
has resulted in algal blooms, anoxia and losses in biodiversity (Anderson
et al., 2002; Meyer-Reil and Köster, 2000; Nixon, 1995). Management
strategies for the reduction of nutrient inputs have been in place globally
for several decades, but this effort alone has not been able to reverse

* Corresponding author. Macquarie University, NSW, 2109, Australia.

E-mail address: giulia.filippini@mq.edu.au (G. Filippini).

https://doi.org/10.1016/j.envpol.2022.120614
Received 26 May 2022; Received in revised form 17 October 2022; Accepted 4 November 2022
Available online 7 November 2022
0269-7491/© 2022 Elsevier Ltd. All rights reserved.
G. Filippini et al.
nutrient enrichment and recover ecological functions (Duarte and
Krause-Jensen, 2018). Additional strategies that promote the decom­
position of organic matter and remineralisation of nutrients are needed
to recover the health of these degraded ecosystems.
In particular, the loss of more than 85% of shellfish reefs globally has
meant of decline of their capacity to regulate water quality and process
nutrients (Beck et al., 2011). Shellfish such as oysters and mussels are
benthic-pelagic couplers, filtering nutrients suspended in the water
column and transferring them to benthic communities by assimilation in
their tissue or the release of faeces and pseudofaeces (termed bio­
deposits). Moreover, biodeposits that settle on the surface of surround­
ing sediments are rich in organic carbon (C), N and P. They promote
sediment microbial metabolism, thus increasing oxygen consumption,
the release of inorganic nutrients such as ammonia (NH+ 4 ), nitrates
(NO-3) and phosphates (PO3- 4 ) (Christensen et al., 2003; Kellogg et al.,
2013; Newell, 2004). While some of these inorganic nutrients are uti­
lised by pelagic and benthic primary producers, others can be tempo­
rarily or permanently removed from the system through sediment burial
and coupled nitrification-denitrification that produces dinitrogen gas
(N2) (Herbert, 1999; Newell et al., 2002). This form of N diffuses into the
atmosphere and thus it is unavailable for primary producers. Further­
more, recent studies have shown that shellfish can enhance denitrifi­
cation in marine coastal systems by hosting denitrifying bacteria in their
guts and shells (Arfken et al., 2017; Caffrey et al., 2016; Ray et al., 2019;
Svenningsen et al., 2012). Hence, the cultivation and harvesting of filter
feeding bivalves has been recognised as a bioremediation method to
remove excess nutrients (Gifford et al., 2007; Onorevole et al., 2018;
Petersen et al., 2014). Moreover, shellfish restoration strategies aiming
to recover the ecosystem service they provide are burgeoning
worldwide.
Even though shellfish generally promote efficient nutrient cycling
and enhance denitrification as outlined above, there is also some evi­
dence showing the opposite. For example, in hypoxic areas where the
exchange of water is low or with limited capacity to process nutrient
inputs, the introduction of reef-forming shellfish has been shown to
contribute to further sediment eutrophication and overwhelm the sys­
tem by directly excreting NH+ 4 or enhancing its release from organic-
enriched sediments through the addition of biodeposits (Erler et al.,
2017; Hoellein and Zarnoch, 2014; Lee et al., 2011; Mortazavi et al.,
2015). Moreover, in these areas where the water resident time is high,
the presence of extensive and densely packed shellfish (e.g. intensive
farms) can deplete not only the resultant phytoplankton but also
planktonic larvae biomass of numerous species, thereby reducing the
functioning and recruitment of wild populations while affecting benthic
communities due to excessive loading of organic material in the sur­
rounding sediments (Jiang and Gibbs, 2005; McKindsey et al., 2011;
Smaal et al., 2013). Thus, in order to introduce or re-introduce shellfish
into coastal systems sustainably (where the ecological carrying capacity
of the area will not be exceeded), it is important that restoration and
aquaculture managers consider shellfish density/size as well as
site-specific characteristics (e.g. nutrient levels, natural primary pro­
ductivity, and hydrodynamic conditions). So far, no studies have
directly assessed the effects of environmental context on the capacity of
shellfish to modulate nutrient cycling (Ray and Fulweiler, 2021). We
propose that local conditions that affect sediment stabilisation and
oxygenation, such as wave exposure (Almroth et al., 2009), tidal regime
(Joye, 1993; Laima et al., 2002), temperature (Herbert, 1999; Thamdrup
et al., 1998) and sediment grain size (Benelli et al., 2019; Serpetti et al.,
2016), can affect the interactions between shellfish and surrounding
sediments, affecting nutrient cycling. Consequently, to support the
development of successful bioremediation tools, it is necessary to
disentangle environmental factors that influence how reef-forming
shellfish affect nutrient cycling.
Moreover, the degree of efficiency with which reef-forming shellfish
process nutrients might also depend on taxonomic variation. For
example, Tenore and Dunstan (1973) showed increased filtration and
2
Environmental Pollution 316 (2023) 120614
biodeposition rates in mussels compared to oysters; and Grenz (1989)
indicated that mussels’ biodeposits had higher organic content than
oysters’. Additionally, Hawkins et al. (1998) reported that oysters are
less efficient than mussels in the selection and digestion of organic
particles, resulting in lower rates of energy gain and nutrient assimila­
tion. On the other hand, a recent study conducted by Barrett et al. (2022)
revealed that rates of nitrogen removal by area via bioextraction and
sediment denitrification were similar in cultivated oysters and mussels.
Similarly, Ray and Fulweiler (2021) did not find significant differences
in the effects of two species of oysters (Crassostrea virginica and C. gigas)
on nutrient cycling. Meta-analysis can help reconcile these seemingly
contrasting results and understand whether these differences in nutrient
processing might be due to shellfish taxa or to the different environ­
mental conditions of each study.
Here, we combined qualitative and quantitative reviews to summa­
rize global knowledge of the effects of reef-forming shellfish, namely
oysters and mussels, on biogeochemical cycles in marine coastal eco­
systems. First, we reviewed the capacity of reef-forming shellfish to
drive denitrification on their shell and in tissues. Second, we (i) assessed
if reef-forming shellfish significantly alter metabolism and nutrient
cycling in surrounding sediments via meta-analysis; and (ii) determined
how environmental factors such as grain size (muddy vs sandy sedi­
ments), seasonality, water body type (i.e. lagoon, distributary channel,
gulf and bay) and tidal position affect the interactions between reef-
forming shellfish and sediment function. We predicted that sediments
surrounding shellfish would have higher sediment oxygen demand
(SOD), nutrient regeneration (fluxes releasing to the water column), and
nitrogen removal than sediments far from shellfish. In addition, we ex­
pected that different shellfish taxa would similarly affect benthic
metabolism and nutrient cycling in surrounding sediments, as observed
in Barrett et al. (2022) and Ray and Fulweiler (2021).
2. Methods
2.1. Literature search and inclusion criteria
We reviewed literature on the role of reef-forming shellfish (mussels
and oysters) on benthic metabolism and nutrient cycling in marine
systems using Scopus and Web of Science. The search terms included
(‘oxygen*, SOD*, sediment-oxygen-demand*, oxygen-flux*, benthic-
metabolism*, nutrient*, nutrient-cycl*, nutrient-flux*’) and (‘shellfish*,
mussel*, bivalve*, oyster*’) in (‘coast*, estuary*, marine*, lagoon*,
gulf*’) not (‘freshwater*’). Searches were conducted during June
2020–June 2021. Reference lists of these studies were checked to
include articles not recovered by our literature search (i.e. theses or
dissertations). After excluding results from unrelated research areas and
removing duplicate articles, we obtained 3773 records (Fig. S1). We
then screened titles and abstracts to select articles that evaluated the
effects of shellfish on (i) benthic metabolism (SOD) as a measure of
biological aerobic metabolism and chemical oxidation in the sediment
(Wang, 1980); and/or (ii) nutrient cycling as inorganic nutrient fluxes
- 3-
between sediments and water column (NH+ 4 , NO3, PO4 , N2 products
from bacterial aerobic and anaerobic metabolism). As a result, 81 re­
cords were selected, including 53 studies that compared benthic pro­
cesses in sediments surrounding shellfish reefs and aquaculture farms
with sediments far from them, and 22 studies that evaluated nutrient
cycling on the shellfish (Fig. S1).
In subsequent filtering, studies were excluded if fluxes were calcu­
lated without using incubation methods (i.e. Fick’s equation). This is
because modelled fluxes only consider the diffusion coefficient and do
not account for volumes and sampling times that provide more accurate
measures for cross-study comparisons (Harmesa and Wahyudi, 2020;
Roth et al., 2019). We also excluded studies that measured denitrifica­
tion using the Isotope Pair Technique (IPT) method, as it requires the
addition of N isotopes and their rates are generally underestimated (Eyre
et al., 2002; Ray et al., 2021). When several studies were based on the
G. Filippini et al.
same data, duplicate data was excluded. This resulted in a total of 18
studies evaluating nutrient cycling on the shellfish reefs (Appendix A).
However, due to the lack of consistency in the controls used between
studies (e.g. water only, bare sediments, dead oysters, shell biofilm),
meta-analyses were not possible. For this reason, we assessed general
patterns of nutrient cycling on shellfish by calculating the proportion of
studies reporting influx or efflux for each variable considered (SOD,
- 3-
NH+4 , NO3, PO4 , N2) and mean fluxes to assess shellfish contribution to
nutrient cycling. Means were obtained from comparable studies that
measured fluxes in μmol m− 2 h− 1 (the most common unit reported),
with values reported in μmol g− 1 h− 1 or in μmol individ− 1 h− 1 excluded.
In contrast, there was a general agreement between studies on the
control used when assessing biogeochemistry on sediments around
reefs, as most of them included sediments far from reefs as controls.
Hence, meta-analyses were done on 32 studies (Appendix A) after
removing studies where: (a) a control site was not present or was not
appropriate (i.e. presence of macroalgae/seagrass on the sediment); (b)
sediments were manipulated with organic material or biodeposit addi­
tions; (c) replicates were not present; and/or (d) data were reported as a
correlation or were not readable and/or extractable.
2.2. Data extraction for meta-analysis of benthic processes in sediments
surrounding shellfish
For each of the 32 studies in the meta-analyses, we extracted sample
size, mean and standard deviation (SD) for oxygen and nutrient fluxes in
sediments surrounding shellfish (treatment) and in control sediments at
least 15 m away from them. When data such as means and errors were
not reported in the text or tables of the study, we extracted those from
plots using WebPlotDigitizer version 4.4. If a study had multiple mea­
sures through time or space, we extracted them all (the effect of multiple
measures extracted from the same study was accounted for in the models
as specified below). If a study reported a range of sample sizes, we used a
conservative approach by selecting the lower sample size reported (e.g.
if “n = 3–4”, we used 3); while, if a study did not specify sample size, we
assumed a sample size equal to 2 (minimum number of replicates for
calculating mean and error). All nutrient fluxes were converted to μmol
m− 2 h− 1 to allow comparisons between studies. In addition, all standard
errors (SE) were converted to SD.
To determine how environmental factors affect the interactions be­
tween shellfish and sediment function, we also recorded for each study
the (i) sediment type (muddy or sandy) – i.e. when mud or sand is ≥ 50
weight percent of the sediment, (ii) the season when the experiment
took place, (iii) water body type of the system (distributary channel,
lagoon, and gulf/bay), and (iv) position relative to tidal height (inter­
tidal and subtidal) – where available. Based on the morphological
characteristics of the water bodies in the analysed studies, we defined
and grouped them into the following categories: (a) distributary channel
- water system connected to the sea/ocean through a river/s; (b) lagoon -
coastal water body separated, intermittently, or constantly connected to
the sea through one or more narrow mouth/s; and (c) gulf and bay –
coastal area of ocean/sea partly surrounded by land. The categorization
employed was based on a visual recognition using Google Maps. When
general information about the sediment type or specifics of grain size
distribution was not reported in the studies, we characterised the site
from information in other studies done at the same location.
For each data point extracted, we used Hedge’s standard mean dif­
ference (SDM) to estimate effect sizes and variance of fluxes (Hedges,
1981). Forest plots were constructed for each response variable using
the ‘forest’ function in metafor package (Viechtbauer, 2010) to show the
individual effect size and sample variance of each study. All analyses
were done in R version 4.1.0.
We assessed publication bias for each response variable by checking
whether there was a significant correlation between effect sizes (SMD)
and sample sizes using funnel plots (Zwetsloot et al., 2017). Sensitivity
analyses were also performed using the ‘leave-one-out’ method to detect
3
Environmental Pollution 316 (2023) 120614
if effects were driven by any single data point (Borenstein et al., 2021).
Funnel plots indicated no publication bias for all variables assessed
(Fig. S2). Furthermore, results from sensitivity analysis conducted for
each response variable showed that results reflected patterns from a
series of datapoints, rather than being influenced by single datapoints
(Table S1).
We tested how the different shellfish species, functional group
(oyster and mussel) and habitat type (farm vs reef) affected SOD and
nutrient fluxes in surrounding sediments with a multi-level model using
function ‘rma.mv’ from the metaphor package (Viechtbauer, 2010). Each
model included a fixed factor (shellfish species = 6 levels; functional
group = 2 levels; and habitat type = 2 levels) and a random factor
(‘trial’) nested in ‘study identity’ to account for non-independence of
multiple data points extracted from the same study (Noble et al., 2017).
Models were run without the intercept to test whether there were sig­
nificant differences between treatment and controls at each level of the
factor considered. To evaluate for statistically significant differences
among shellfish species, functional groups and habitat types, we con­
ducted a post-hoc test by using the function ‘ghlt’ in multcomp package
(Hothorn et al., 2008). Specifications of the models used are summarised
in equation S1.
We then assessed if these patterns were affected by the environ­
mental context, including sediment grain size (sandy vs muddy), sea­
sonality (summer, autumn, winter and spring), water body type
(distributary channel, lagoon, and gulf/bay), and tidal zone (intertidal
and subtidal) by adding them to the models described above - (Equation
S2). Interactions between environmental factors and shellfish taxa and
habitat types could not be investigated due to insufficient data. To
measure how seasons might affect SOD and nutrient cycling in sedi­
ments surrounding shellfish, studies conducted in locations charac­
terised by only two seasons (i.e. tropics) were excluded. Since tropical
locations do not present the same four seasons as temperate areas, but
rather only wet and dry, it was deemed inappropriate to include studies
conducted in tropical areas with those from temperate regions. More­
over, an assessment of the effect of seasons in tropical zones was not
possible due to a low number (two) of such studies. Orchard plots were
used to visualise effect sizes of different categories within each envi­
ronmental moderator using function ‘orchard_plot’ through the OrchaRd
package (Noble, 2021). As there were no differences between shellfish
species and functional groups or between habitat types (except for NH+ 4
fluxes; see results below), effects of environmental factors on the SOD
and nutrient fluxes were analysed combining all taxonomic groups.
Post-hoc tests showed that there were differences between habitats only
for NH+ 4 fluxes, but as studies assessing NH4 fluxes were mostly done in
+
farms (more details in results), it was not possible to test for moderators
for each habitat type. Hence, they were also combined.
3. Results
The majority of studies (94%) included in the qualitative and meta-
analysis were within temperate areas, with only three studies reported
from tropical zones (French Polynesia). Results showed geographical
bias as most studies were conducted in the Northern hemisphere (85%),
with the majority of these being from North America (61%) and Europe
(34%, Fig. S3). Of the studies measuring fluxes on shellfish, 52% focused
on oysters and the remaining 48% on mussels. Similarly, 57% of studies
assessing fluxes on sediments around shellfish were associated with
oysters (70% of which were conducted in North America), and 43% with
mussels (of which 60% were undertaken in Europe, Fig. S4). Overall,
C. virginica and Mytilus galloprovincialis were the most studied species,
making up 35% and 15% of the studies respectively. These were fol­
lowed by C. gigas and Mytilus edulis (both representing 14% of studies,
Fig. S3). While 70% of the studies were undertaken in shellfish aqua­
culture sites, the remainder were completed in natural or restored
shellfish reefs. Interestingly, more than 67% of the studies assessing
- 3-
sediment oxygen demand, NH+ 4 , NO3 and PO4 fluxes were done in
G. Filippini et al.
aquaculture farms, while 79% of studies assessing denitrification were
done on shellfish reefs (Fig. S4).
3.1. Benthic metabolism and nutrient fluxes on shellfish reefs and in
surrounding sediments
More than 70% of the 18 studies in our qualitative review that
evaluated nutrient cycling on shellfish measured metabolism (oxygen
consumption) and the excretion of NH+ 4 . Oxygen consumption had a
magnitude of 2213.69 ± 480.94 μmol m− 2 h− 1. About 30% of these
studies considered the efflux and influx of NO-3 and PO34 , while 20%
-
focused on N2 (Table S2). All 18 studies reported positive fluxes of NH+ 4,
and N2 from shellfish (i.e. efflux, or release from shellfish to water col­
umn), at 842.76 ± 174.82 and 302 ± 125.90 μmol N2 m− 2 h− 1 respec­
tively. In contrast, there were mixed results for NO-3, with half the
datapoints (4 out of 8) indicating an influx, and the other half reporting
an efflux (Table S3). Mean and SD calculations for NO-3 and PO3- 4 were
not possible due to the different units of measurement used between
studies (i.e. some standardised fluxes by habitat area or volume, while
some others by dry weight).
From the 32 studies considered for the meta-analyses, more than
40% assessed benthic metabolism and the release of NH+ 4 on sediments
surrounding shellfish reefs and farms, about 30% measured NO-3 and
PO34 fluxes, and 25% evaluated denitrification (Table S4). Overall, meta-
-
3-
analyses showed that SOD and NH+ 4 , PO4 and N2 effluxes were greater in
sediments near than far from shellfish (Fig. 1, Table 1). Specifically,
sediments surrounding shellfish had 1.38 ± 0.19 times greater SOD than
3-
control sediments. NH+ 4 , PO4 and N2 effluxes were 1.49 ± 0.29, 1.26 ±
0.28, 0.59 ± 0.25 times greater in sediments close to than those far from
shellfish reefs/farms. By contrast, NO-3 was taken up at similar rates by
sediments near and far from shellfish (Fig. 1; Table 1). Post-hoc tests did
not show differences between different shellfish species and functional
groups (oysters and mussels, Table S5); hence the assessment of mod­
erators was done for all taxa combined. On the other hand, differences
between shellfish farms and reefs were only found for NH+ 4 fluxes
(Table S5). Specifically, the release of NH+ 4 from sediments surrounding
shellfish aquaculture was significantly higher than control sites (1.80 ±
0.29; p-value < 0.001); while in sediments surrounding reefs NH+ 4 fluxes
Fig. 1. Effect size (SMD ± CI) of sediment oxygen demand (SOD), ammonia (NH+
surrounding shellfish (oyster only studies were found for N2 fluxes) when compared to sediments far from shellfish. Dotted line shows an effect size equal to 0. Only p-
values that are statistically significant (p-value < 0.05) are shown in bold.
4
Environmental Pollution 316 (2023) 120614
were similar to sediments far from the reefs (− 0.09 ± 0.61; p-value =
0.881). Although differences between shellfish aquaculture and reefs
were found for this nutrient (Table S5), moderators were assessed by
pooling the data together since there were only five studies found for
reefs (Fig. S4).
3.2. Environmental moderators of shellfish effects on benthic metabolism
and nutrient fluxes in surrounding sediments
Sediments surrounding shellfish reefs and farms had greater SOD and
release of NH+4 than control sediments in sandy and muddy sediments,
intertidal and subtidal zones and seasons (Figs. 2 and 3, Table 1).
However, results varied between water body types. Both SOD and
release of NH+ 4 in sediments surrounding shellfish were significantly
greater than controls in lagoons and gulf/bays, but not in distributary
channels, although these differences might be influenced by a lack for
power in distributary channels given the lower number of studies per­
formed in this water body (Figs. 2 and 3, Table 1). By contrast, NO-3
influxes in sediments near and far from shellfish were similar in all the
environmental contexts (Fig. 4, Table 1). Moreover, the release of PO34
-
was found to be greater in sediments surrounding shellfish than control
sediments regardless of sediment type or tidal zone (Fig. 5, Table 1), but
only in summer and autumn and in lagoon and gulf/bay systems
(although one study was found in a distributary channel, Fig. 5, Table 1).
N2 effluxes were 0.68 ± 0.32 times greater in sandy sediments sur­
rounding oysters than control sediments, but did not differ in muddy
sediments (Fig. 6, Table 1). The release of N2 from sediments sur­
rounding oysters was 0.99 ± 0.39 times greater than controls in sum­
mer, while no differences were found during the other seasons (Fig. 6,
Table 1). N2 effluxes from sediments around oysters were also greater
than control sites in lagoons and intertidal systems (Fig. 6, Table 1).
However, the lack of effects for many of these groups might be due to the
low number of studies available.
4. Discussion
The continuing eutrophication of coastal marine ecosystems is a
global issue that needs to be addressed with urgency. Biogenic habitats
- 3-
4 ) flux, nitrate (NO3) flux, phosphate (PO4 ), dinitrogen gas (N2) in sediments
G. Filippini et al. Environmental Pollution 316 (2023) 120614

have been shown to play an essential role in nutrient processing through

Meta-analysis comparing benthic metabolism and nutrient fluxes between sediments near and far from shellfish from all studies (overall effect size) and at different sediment type, season, water body type, and tidal type,
4 ), nitrate (NO3 ), phosphate (PO4 ), and dinitrogen gas (N2) fluxes. Distributary

z-value
assimilation (filter feeding/roots absorption), burial and enhanced

− 0.41
2.32

2.16

2.54

2.21

2.53
0.86

1.08
0.40

0.37

0.71
0.00
denitrification. For example, mangrove forests were shown to release N2
from 1.9 to 9.25 μmol N2 m− 2 h− 1 (Alongi, 1996; Kristensen et al., 1998;
Rivera-Monroy et al., 1995). Higher denitrification rates (> 50 μmol N2

0.25
0.49
0.32
0.58
0.56
0.39
0.55
0.32
0.64
1.24
0.90
0.27
m− 2 h− 1) have also been found in salt marsh and seagrass environments

SE
(Aoki and McGlathery, 2018; Caffrey et al., 2007; Garcias-Bonet et al.,
Estimate 2018; Sousa et al., 2012; Velinsky et al., 2017). In this study, we esti­

− 0.38
mated that denitrification rates on shellfish can be at least an order of
0.59
0.42
0.68
0.63
0.23
0.99
0.20
0.70
0.45
0.00

0.69
magnitude greater than those observed in many other biogenic habitats,
N2

with a mean of 302 ± 125.90 μmol N2 m− 2 h− 1. Likewise, we estimated

that the presence of oysters stimulates the release of up to 60% more N2
z-value

4.46
3.56
2.49

3.53
2.91
3.78

2.08
3.50
2.63
from the surrounding sediments, similar to that found in a previous
1.49
1.91

0.13
study (Ray and Fulweiler, 2021). The increases in SOD by 1.38 times
close to shellfish are evidence of a surge in aerobic microbial processes,
3-

supporting the mentioned increases in nutrient regeneration. These re­

0.28
0.39
0.44
0.66
0.75
0.43
0.51
0.37
1.34
0.55
0.33
0.58
SE

sults highlight that shellfish are important for removing N from coastal
ecosystems because denitrification can be enhanced both by microbes
on shellfish and by shellfish stimulating microbial activity in nearby
Estimate

1.26
1.37
1.01
0.98
1.44
1.53
1.49
1.39
0.18
1.14
1.17
1.52

sediments.
PO3-
4
−

Interestingly, qualitative results showed that shellfish can uptake

large amounts of oxygen (~2000 μmol m− 2 h− 1) and excrete NH+ 4 at
~800 μmol m− 2 h− 1. Moreover, they can increase the release of NH+ 4 and
z-value

− 0.77
− 1.09

− 0.27
− 0.90
− 1.45
− 0.17

− 1.05
0.03
0.21
0.95

0.51
0.56

PO34 from sediments to the water column by up to 1.49 times. If optimal

-

biological and environmental conditions exist (i.e. an aerobic environ­

including showing estimate (Hedge’s g), standard error (SE), and z-value for variables of sediment oxygen demand (SOD), ammonia (NH+

-
ment adjacent to an anaerobic one), the generated NH+ 4 /NO3 is con­
0.34
0.45
0.51
1.73
0.06
0.51
0.64
0.44
1.62
0.49
0.47
0.47

verted into N2 by coupled nitrification-denitrification reactions (Kellogg

SE

et al., 2014; Newell, 2004). Inorganic N that is not transformed will

diffuse into the water column, where it can drive phytoplankton growth
Estimate

and could potentially lead to algal blooms, eutrophication and anoxic

− 0.26
− 0.49

− 0.14
− 0.57
− 0.64
− 0.28

− 0.49
0.02
0.36
0.04

0.25
0.26

events, especially in systems where the mixing is limited or where the

NO-3

oxygen is already somewhat depleted. Previous studies have shown that

shellfish may be able to counter this increased phytoplankton biomass
z-value

through filtration (Cranford et al., 2011; Soto and Mena, 1999), but this
5.21
4.25
3.30
3.41
2.50
4.00
2.78
3.13

4.18
5.49
2.34
0.95

top-down control can have both positive and negative impacts on

ecosystem services depending on site-specific characteristics (Smaal
et al., 2019; van der Schatte Olivier et al., 2020). Positive effects are
0.29
0.38
0.41
0.69
0.50
0.37
0.48
0.38
1.29
0.47
0.37
0.44

likely to occur at optimal shellfish density in more enriched and shallow

SE

areas, where shellfish filtration can act as a biofilter mitigating eutro­

phication and improving water quality (Jansen et al., 2019; Lindahl,
Estimate

2011; Schroder et al., 2014). By reducing turbidity and increasing light

1.49
1.61
1.36
2.34
1.25
1.48
1.32
1.20
1.23
1.97
2.01
1.03
NH+
4

penetration, shellfish can enhance benthic productivity of important

habitats like seagrass (Sharma et al., 2016; Smyth et al., 2018; Wall
et al., 2008), which in turn improves water quality (by reducing the
stands for distributary channel. Significant differences are outlined in bold.

z-value

7.70
4.48
6.57
2.27
3.92
4.86
3.32
5.83

5.29
5.57
5.25

availability of nutrients for phytoplankton) and provides food and

0.71

habitat for many species (Newell et al., 2002; Petersen et al., 2019;
Sandoval-Gil et al., 2016; Zertuche-González et al., 2009). Additionally,
through the filtration of phytoplankton, shellfish accumulate nutrients
0.18
0.24
0.26
0.50
0.39
0.29
0.38
0.23
0.65
0.31
0.25
0.27
SE

(N and P) that can temporarily be subtracted and permanently removed

from coastal environments if/when harvested (Carmichael et al., 2012;
Cerco and Noel, 2007). Interestingly, a recent study has shown that
Estimate

1.38
1.10
1.69
1.13
1.52
1.41
1.22
1.35
0.46
1.63
1.36
1.41

shellfish can remove 314–581 kg N ha− 1 yr− 1 via harvesting, which

SOD

provides a higher contribution in the reduction of N than sediment

denitrification beneath farms (Barrett et al., 2022). On the other hand, in
oligotrophic systems or in areas with greater flushing (highly hydrody­
Overall effect size

namic systems), large densities of shellfish can extremely deplete

Distributary

phytoplankton, resulting in an increase of non-filtered primary pro­

Intertidal
Gulf/Bay
Summer

Subtidal
Autumn

ducers (picoplankton) and a reduction of food for themselves and for

Lagoon
Muddy

Winter
Spring
Sandy

other filter-feeders (Grant and Pastres, 2019; Smaal et al., 2013). This
would therefore shift benthic communities from filter to deposit feeders,
while reducing recruitment of wild shellfish and other species (Cranford,
Water body type

2019; Gibbs, 2007; van Stralen and Dijkema, 1994). Furthermore, Fer­
Sediment type

riss et al. (2019) indicated that shellfish aquaculture can reduce seagrass
Seasonality

Tidal type

density, biomass and reproduction in areas directly underneath and

Table 1

immediately surrounding farms, mainly due to space and light limita­

tion. Thus, to achieve successful bioremediation, it is essential to

5
G. Filippini et al. Environmental Pollution 316 (2023) 120614

Fig. 2. Effect size (SMD ± CI and Prediction interval) of sediment oxygen demand (SOD) in sediments surrounding shellfish when compared to sediments far from
shellfish for the four selected environmental factors: (a) sediment type, (b) seasonality, (c) water body type, and (d) tidal type. Dotted line shows an effect size equal
to 0. Individual effect size points on the right side of the dotted line indicates a greater SOD from the sediments surrounding shellfish, while individual effect size
points on the left side suggests a less SOD. Point estimates, 95% confidence intervals and 95% prediction intervals are represented by shaded points, bold black error
bars and black horizontal lines. Only p-values that are statistically significant (p-value < 0.05) are shown in bold.

consider environmental characteristics of the site and set a threshold on
the scale of restoration/introduction (i.e. the correct density of shellfish)
that will positively affect interactions between shellfish and surrounding
habitats.
While restored shellfish reefs and aquaculture farms may have
different impacts on sediment functions due to their structural and
ecological differences, we found that this was only true for NH+ 4 fluxes.
Findings indicated that aquaculture farms increased NH+ 4 fluxes in sur­
rounding sediments, while this was not observed for shellfish reefs. This
difference might be due to shading of farms preventing the recycle of
nutrients via primary productivity, and/or to higher shellfish density
and size in aquaculture sites. As mentioned, a larger density of shellfish
might lead to overgrazing of phytoplankton, which can result in a higher
deposition of organic material in the surrounding sediments (Weitzman,
2019). The large accumulation of biodeposits can result in higher NH+ 4 sediment effluxes of NH+
release through mineralisation as well as depletion of oxygen and
release of H2S near and under shellfish farms (Callier et al., 2009;
McKindsey et al., 2011). It should be noted that these results might be
due to a low power to detect effects of reefs, given that only a small
number of studies (n = 5) addressing NH+ 4 cycling were conducted in
shellfish reefs. Similarly, the majority of studies focusing on benthic
metabolism, NO-3 and PO34 fluxes were undertaken in shellfish aqua­
-
culture and in oyster reefs for denitrification. Thus, we suggest that
studies assessing benthic metabolism and nutrient cycling in both
shellfish aquaculture and reefs need to expand the variables measured
(including shellfish density and reef/farm size) to understand the dif­
ferences between them.
Although oyster and mussel species differ in their capacity to ingest,
assimilate and reject various quantities and qualities of food particles,
resulting in different compositions of their biodeposits (Grenz, 1989;
Hawkins et al., 1998; Tenore and Dunstan, 1973), no differences were
detected in benthic metabolism and nutrient regeneration of sediments
surrounding oyster and mussel species. This result is in accordance with
our hypothesis and with two previous studies which indicated that
3-
4 and PO4 were comparable among oyster
species, and that cultivated oysters and mussels similarly enhance
sediment denitrification (Barrett et al., 2022; Ray and Fulweiler, 2021).
However, we could not assess whether mussels would affect denitrifi­
cation in the same way. This is because mussel studies typically estimate
N2 fluxes using the IPT method, which produces results that are not

6
G. Filippini et al.
Fig. 3. Effect size (SMD ± CI and Prediction interval) of ammonia (NH+ 4 ) flux in sediments surrounding shellfish when compared to sediments far from shellfish for
the four selected environmental factors: (a) sediment type, (b) seasonality, (c) water body type, and (d) tidal type. Further details as in Fig. 2.
comparable to the N2/Ar technique (Eyre et al., 2002). Despite this, our
results suggest that the introduction of either mussels or oysters into
degraded systems can enhance benthic metabolism and nutrient cycling
at similar rates.
It is important to note that these results may have been influenced by
geographical location since the majority of studies on mussels and
oysters were undertaken in the Northern hemisphere (in Europe and
North America respectively), with minimal research conducted in other
countries such as Australia and South Africa. Moreover, Chesapeake
Bay, Baltic Sea and Northern Adriatic Sea (where most of the studies
were completed) are among the coastal areas most impacted by nutrient
loadings in the world (Malone and Newton, 2020). While the presence of
shellfish in these areas has been shown to significantly change nutrient
cycling, this may not always be the case for areas characterised by fewer
nutrient inputs (Jansen et al., 2012; Stenton-Dozey et al., 2011).
Therefore, research focusing on how benthic metabolism and nutrient
cycling are affected by either mussels or oysters under a variety of
environmental conditions is needed to shed light on the global relevance
of these results.
As expected, SOD and nutrient regeneration (releases of NH+ 4 and
3-
PO4 ) increased considerably in lower energy systems (i.e. lagoons),
probably due to the higher accumulation of biodeposits in the sur­
rounding sediments (Mazouni et al., 1996; Nizzoli et al., 2005).
7
Environmental Pollution 316 (2023) 120614
However, these variables were also found to be significantly higher in
more open systems (i.e. gulf and bay), suggesting that the presence of
shellfish affects nutrient fluxes in sediments at a range of hydrodynamic
conditions. Similarly, results from this study did not show differences
3-
between tidal level for SOD and nutrient fluxes (NH+ 4 and PO4 ), high­
lighting that the presence of shellfish can have a significant effect on
sediment functions in both intertidal and subtidal systems. Thus, even if
sediments in intertidal systems are subjected to greater environmental
pressure due to drastic changes in light intensity, temperature, salinity,
oxygen availability, or hydrodynamics during high and low tides (Hou
et al., 2007; Nielsen et al., 1990; Rysgaard et al., 1999), the increase in
organic material through shellfish biodeposits might still promote mi­
crobial metabolism and nutrient regeneration in these systems. Alter­
nately, this increase in SOD and nutrient fluxes could be due to excretion
and bioturbation activity of an increased infauna presence (such as de­
posit feeding polychaetes) in sediments around shellfish (Bugnot et al.,
2022; Giles et al., 2006). In terms of the seasonal differences observed in
nutrient fluxes (release of PO3- 4 and N2), results showed expected pat­
terns, as benthic metabolism and nutrient cycling are influenced by the
increase in water temperatures during warmer seasons (Akomeah and
Lindenschmidt, 2017; Malinverno and Martinez, 2015). On the other
hand, our results have shown that shellfish increased SOD and the
release of NH+ 4 from surrounding sediments in all seasons. Thus, this
G. Filippini et al.
Fig. 4. Effect size (SMD ± CI and Prediction interval) of nitrate (NO-3) flux in sediments surrounding shellfish when compared to sediments far from shellfish for the
four selected environmental factors: (a) sediment type, (b) seasonality, (c) water body type, and (d) tidal type. Further details as in Fig. 2.
result might suggest that mineralisation of organic material in sediments
around shellfish might be more influenced by physico-chemical vari­
ables other than temperature (i.e. quality, quantity of OM or bio­
deposits) or by the presence of infauna found to be greater in sediments
around shellfish (Bugnot et al., 2022; Giles et al., 2006).
Meta-analysis results showed that oysters enhance denitrification in
sandy lagoons. These findings are not surprising as the deposition of
labile organic matter via biodeposits in sediments can be enhanced in
more enclosed systems, where the mixing and resuspension of organic
material is limited (Hartstein and Stevens, 2005; Humphries et al.,
2016). Moreover, sandy sediments are generally characterised by high
permeability and great oxygenation, hence the deposition of biodeposits
can stimulate microbial metabolism and subsequently decrease
oxygenation, generating favourable oxic/anoxic transitions for deni­
trifying processes (Ahmerkamp et al., 2017; Cornwell et al., 1999).
Although denitrification in muddy sediments and other water bodies
considered (gulf/bay and distributary channel) presented a lower
number of studies (potentially masking evidence of denitrification in
these environmental context), results suggest that introducing oysters
into lagoons or other systems with sandy sediments can efficiently
remove N from these environments, thereby improving water quality.
Future research could consider variables such as shellfish size, density,
reef/culture age, light intensity, and water quality/nutrient gradients to
8
Environmental Pollution 316 (2023) 120614
better identify environmental conditions that can enhance bioremedia­
tion. Additionally, as we still know little of the mechanisms by which
shellfish affect surrounding sediments (if it is via biodeposit additions or
if their presence changes microbial biodiversity), we suggest that these
analyses should be linked with microbial communities and gene markers
of environmental DNA to fully understand how shellfish affect nutrient
cycling (Lindemann et al., 2016; Thomsen and Willerslev, 2015).
In summary, this is the first study showing that, overall, environ­
mental factors such as season, sediment composition and water body
type can modulate the effects of shellfish reefs on sediment function,
with consequences for biogeochemical cycling. Moreover, the effects of
shellfish on sediment function depend on shellfish density, reef/farm
size and other site-specific conditions which can tip the scale towards
negative effects on ecosystem services. Hence, in order to efficiently use
shellfish to remediate excess nutrients and improve water quality, these
parameters need to be considered and further studies ae needed to
establish thresholds in shellfish densities and restoration/farm size.
Currently, site selection procedures for marine ecosystem restoration
have been limited to consider the environmental context suitable for the
survival of the restored organism (Beseres Pollack et al., 2013; Lester
et al., 2020). However, the results of this study showed that the recovery
of ecosystem services such as nutrient regeneration depends on envi­
ronmental context, hence site selection should also include information
G. Filippini et al.
Fig. 5. Effect size (SMD ± CI and Prediction interval) of phosphate (PO3-
4 ) flux in sediments surrounding shellfish when compared to sediments far from shellfish for
the four selected environmental factors: (a) sediment type, (b) seasonality, (c) water body type, and (d) tidal type. Further details as in Fig. 2.
about the environmental conditions that maximise the desired
ecosystem services. Here, we propose that projects aiming to maximise
water quality and N removal delivered by shellfish should include
nutrient levels (e.g. high levels of natural primary productivity), sedi­
ment grain size (e.g. sandy sediments), hydrodynamics (e.g. lagoons
systems), and depth (e.g. shallow water) for site selection. Similarly,
planning for areas suitable for the development of aquaculture farms are
limited to assessing areas with low potential for ecological impacts,
while providing good economic and social benefits (Stelzenmüller et al.,
2017; UNESCO-IOC and European Commission, 2021). If we aim to
maximise the co-benefits of shellfish aquaculture, then planning should
also consider prioritising areas with the environmental conditions that
maximise the delivery of ecosystem services (Gentry et al., 2020). Ul­
timately, strategies that set clear objectives can plan ahead and incor­
porate the knowledge gathered in this study to maximise the delivery of
ecosystem services by shellfish.
5. Conclusions
This study showed that reef-forming shellfish (both oysters and
mussels) can potentially act as bioremediation tools to mitigate eutro­
phication. In the cases analysed in this review and meta-analysis,
shellfish significantly increased oxygen demand, inorganic nutrient
9
Environmental Pollution 316 (2023) 120614
3-
efflux (NH+4 and PO4 ), and denitrification (N2) in the surrounding sed­
iments. Although, the success of this tool does not necessarily depend on
environmental context (i.e. sediments and water body types) with
3- -
regards to SOD and nutrient cycling (NH+ 4 , PO4 and NO3); bioremedi­
ation projects that aim to remove N could improve outcomes by intro­
ducing oysters in lagoons and in systems with sandy sediments. We also
suggest that the planning of sites and spatial scales of shellfish restora­
tion and development of aquaculture farms should consider the envi­
ronmental aspects identified in this study to maximise ecosystem
services provided by shellfish (i.e. nutrient remediation and improve­
ment of water quality).
Credit author statement
Giulia Filippini: Conceptualization, Methodology, Formal analysis,
Data curation, Visualization, Writing – original draft, Writing – review &
editing. Katherine A. Dafforn: Conceptualization, Methodology, Super­
vision, Writing – review & editing. Ana B. Bugnot: Conceptualization,
Methodology, Formal analysis, Supervision, Writing – review & editing.
Funding sources
This research did not receive any specific grant from funding
G. Filippini et al. Environmental Pollution 316 (2023) 120614

Fig. 6. Effect size (SMD ± CI and Prediction interval) of dinitrogen gas (N2) flux in sediments surrounding shellfish when compared to sediments far from shellfish
for the four selected environmental factors: (a) sediment type, (b) seasonality, (c) water body type, and (d) tidal type. Further details as in Fig. 2.

agencies in the public, commercial, or not-for-profit sectors. GF was Copenhagen) and Dr Nina Schäfer (Sydney Institute of Marine Science)
supported by an iMQRES PhD Scholarship awarded through the School for their help during statistical analysis.
of Natural Sciences, Macquarie University.
Appendix A. Supplementary data

Declaration of competing interest

Supplementary data to this article can be found online at https://doi.
org/10.1016/j.envpol.2022.120614.
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
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