A food-web model as a tool for the ecosystem-level management of bivalves in an Atlantic coastal lagoon

Abstract

The Ria de Aveiro is an important coastal lagoon for wildlife in Portugal, where the production of bivalves reaches approximately 2700 tons annually. However, the illegal overfishing of bivalves is frequent in this lagoon, which causes critical changes in the ecosystem. In this study, using a developed food-web model (Ecopath model), the ecological carrying capacity (ECC) and maximum sustained yield (MSY) of the Manila clam, Ruditapes philippinarum were estimated, and the effects of further increases in clam biomass on other species were investigated. The results showed that 1) the current biomass and legal catch of R. philippinarum do not yet exceed the ECC (172.40 tons km-2) or the MSY (86.20 tons km-2 year-1) in Ria de Aveiro; 2) the harvested Manila clams of the MSY represent removing from the ecosystem ∼ 581 tons carbon (C) and ∼83 tons nitrogen (N) annually, with substantial ecological and economic implications; and 3) a further increase in the biomass levels of this species may cause the ecotrophic efficiency of other groups to become unrealistic, potentially leading to decreases in ecosystem transfer efficiency, biodiversity and health. The results here are expected to guide the sustainable development and management of bivalve aquaculture in Ria de Aveiro and the protection of the local environment.

Full text

Marine Environmental Research 190 (2023) 106117
Available online 25 July 2023
0141-1136/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
A food-web model as a tool for the ecosystem-level management of bivalves
in an Atlantic coastal lagoon
Weiwei Jiang
a
,
b
, Francesca Coppola
c
, Zengjie Jiang
a
,
b
,
*
, Rosa Freitas
c
,
**
, Yuze Mao
a
,
b
,
Zhijun Tan
a
, Jinghui Fang
a
,
b
, Jianguang Fang
a
,
b
, Yitao Zhang
d
a
State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao,
266071, China
b
Laboratory for Marine Fisheries Science and Food Production Processes, Laoshan Laboratory, Qingdao, 266200, China
c
CESAM & Department of Biology, University of Aveiro, Aveiro, 3810-193, Portugal
d
Rongcheng Chudao Aquaculture Corporation, Rongcheng, 264312, China
ARTICLE INFO
Keywords:
Ria de Aveiro
Ecopath model
Ruditapes philippinarum
Ecological carrying capacity
Maximum sustained yield
ABSTRACT
The Ria de Aveiro is an important coastal lagoon for wildlife in Portugal, where the production of bivalves
reaches approximately 2700 tons annually. However, the illegal overshing of bivalves is frequent in this lagoon,
which causes critical changes in the ecosystem. In this study, using a developed food-web model (Ecopath
model), the ecological carrying capacity (ECC) and maximum sustained yield (MSY) of the Manila clam, Rudi-
tapes philippinarum were estimated, and the effects of further increases in clam biomass on other species were
investigated. The results showed that 1) the current biomass and legal catch of R. philippinarum do not yet exceed
the ECC (172.40 tons km
−2
) or the MSY (86.20 tons km
−2
year
−1
) in Ria de Aveiro; 2) the harvested Manila
clams of the MSY represent removing from the ecosystem ~ 581 tons carbon (C) and ~83 tons nitrogen (N)
annually, with substantial ecological and economic implications; and 3) a further increase in the biomass levels
of this species may cause the ecotrophic efciency of other groups to become unrealistic, potentially leading to
decreases in ecosystem transfer efciency, biodiversity and health. The results here are expected to guide the
sustainable development and management of bivalve aquaculture in Ria de Aveiro and the protection of the local
environment.
1. Introduction
Bivalve lter feeders, such as mussels, oysters and clams, play key
roles in many estuarine and coastal waters, owing to their high density
(Smaal et al., 2001), extensive ltration capacity (Prins et al., 1996),
enhanced biodeposition (Crawford et al., 2003) and alteration of
nutrient and oxygen uxes (Mao et al., 2006). During the past 50 years,
the world production of bivalves (both capture and aquaculture) has
increased quickly from 1 million tons to 13.2 million tons (Dumbauld
et al., 2009; Dias et al., 2021). Their commercial exploitation has led to
either increased or decreased abundance in many coastal waters, raising
concerns about environmental problems and sustainable development
(H´
eral, 1993; Smaal et al., 1998). Application of the carrying capacity in
the exploitation of natural resources has been used as an approach to
examine environmental sustainability (Smaal et al., 2001).
Coastal lagoons are among the most productive aquatic systems,
supporting a large diversity of habitats that offer optimal niches for
numerous aquatic species (Villanueva et al., 2006). Ria de Aveiro is a
coastal shallow lagoon situated on the northwest coast of Portugal
(40◦38
′
N, 8◦45
′
W). This aquatic ecosystem comprises an area between
66 and 83 km
2
at low tide and high tide (spring tide), respectively, and is
characterized by narrow channels, inner basins and large areas of
mudats (Lillebø et al., 2015). The average depth of Ria de Aveiro is
approximately 1 m, except for navigation channels where dredging
operations are frequently carried out (Dias et al., 2000). The production
of bivalve lter feeders has reached approximately 2700 tons in Ria de
Aveiro annually (Bueno-Pardo et al., 2018). The Manila clam, Ruditapes
philippinarum, is the most abundant clam in this lagoon, representing
* Corresponding author. State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of
Fishery Sciences, Qingdao, 266071, China.
** Corresponding author.
E-mail addresses: jiangzj@ysfri.ac.cn (Z. Jiang), rosafreitas@ua.pt (R. Freitas).
Contents lists available at ScienceDirect
Marine Environmental Research
journal homepage: www.elsevier.com/locate/marenvrev
https://doi.org/10.1016/j.marenvres.2023.106117
Received 10 June 2023; Received in revised form 21 July 2023; Accepted 24 July 2023

Marine Environmental Research 190 (2023) 106117
2
about 50% of the total revenue from the artisanal small-scale bivalve
sheries (Maia et al., 2014; Velez et al., 2015). The abundance of
R. philippinarum accounted for about 41% of the clam species in Ria de
Aveiro (Velez et al., 2015). However, currently, the exploitation of clams
in Ria de Aveiro is continuously increasing, with critical changes in
ecosystems and severe consequences. The catch limitation of clams ur-
gently needs to be estimated based on a shing yield that ensures sus-
tainable harvesting.
The carrying capacity of a natural population is derived from the
logistic growth curve and is dened as the maximum standing stock that
an ecosystem can support in a given time (Smaal et al., 1998). Inglis
et al. (2000) divided carrying capacity into four functional categories, i.
e., physical, production, ecological, and social carrying capacities. On
the ecological level, carrying capacity is approached more holistically
and dened as the stocking or farm density that causes “unacceptable”
impacts on the ecosystem (McKindsey et al., 2006). A holistic approach
is, therefore, important because certain levels of carrying capacity may
be “unacceptable” to other system components; e.g., high stock densities
lead to cascade effects within the trophic structure of the ecological
system (Jiang and Gibbs, 2005; Kluger et al., 2016). On the other hand,
positive effects of bivalve cultivation may also be possible; e.g., the
cultured species provide new habitat structures or increase the food
sources (McKindsey et al., 2006; Meyer, 2014). A food-web Ecopath
model has been proposed to estimate the ecological carrying capacity
(ECC) for use in aquaculture by increasing the biomass of cultured bi-
valves until the ecotrophic efciency becomes unrealistic (i.e., >1) (see
Jiang and Gibbs, 2005; Byron et al., 2011a; 2011b). Ecopath creates a
static snapshot representation of the different compartments of an
ecosystem and their interactions in a specic period, while Ecosim
simulates its dynamic evolution through time and analyzes the effects of
different variables on the ecosystem (Christensen and Walters, 2004;
Han et al., 2018).
Maximum sustained yield (MSY) is dened as the highest production
of food from the sea on a sustained basis year after year (Carmel, 2011).
According to Byron et al. (2011a) and Mace (2001), using half of the
carrying capacity as MSY provides a precautionary approach to aqua-
culture management. Estimating the MSY of aquatic animals is also
essential to meet the objectives of maximizing yield while protecting the
long-term viability of populations and ecosystems. In recent years, re-
searchers have contributed to the understanding of dynamic groups and
the MSY of various kinds of sh species (Sher et al., 2012; Panhwar and
Liu, 2013). However, despite a huge commercial demand for clams, no
published information is available on the MSY of clams in Ria de Aveiro.
The study presented here aims 1) to implement an Ecopath model to
estimate the ECC and MSY of R. philippinarum in the Ria de Aveiro; 2) to
quantify feeding, respiration and excretion rates based on ow-through
experiments to analyze the ecosystem role of this clam species in this
Portuguese coastal shallow lagoon; and 3) to evaluate the possible
impact of a further increase in the Manila clam biomass on other species
groups and possible ecosystemic changes with Ecosim. This research will
contribute to the protection of the ecological environment and provide
basic data for the sustainable management of bivalve farming in Ria de
Aveiro. The results observed here could also be used for other coastal
lagoons or estuaries with similar characteristics (Heymans et al., 2016).
2. Materials and methods
2.1. Model construction
2.1.1. Ecopath model
The Ecopath model was congured to best evaluate the current state
of the ecosystem and then evaluated to estimate clam biomass levels
until dramatic changes to energy uxes occurred, which is dened as the
ecological carrying capacity here (Jiang and Gibbs, 2005). The model
includes a set of linear equations that describe the production of each
functional group:
Bi× (P/B)i×EEi=
n
j=1
Bj× (Q/B)j×DCij +Yi+Ei+BAi
where B
i
and B
j
are the biomasses of group i and group j, respectively;
(P/B)
i
is the production to biomass ratio for group i or total mortality in
steady-state conditions; EE
i
is the ecotrophic efciency, which is dened
as the proportion of the production of group i that is used in the
ecosystem; (Q/B)
j
is the food consumption to biomass ratio for predator
group j; DC
ij
is the fraction of prey i in the stomach content of predator j;
Y
i
is the shery yield of group i; E
i
is the net migration rate; and BA
i
is the
biomass accumulation rate for group i. For each functional group i, the
DC
ij
and at least three of the four basic parameters are required to build
the Ecopath model: B, P/B, Q/B and EE.
A trophic model of Ria de Aveiro was constructed using the software
Ecopath with Ecosim (EwE) 6.5 (Christensen and Walters, 2004) and
was based on a previous model by Bueno-Pardo et al. (2018). The
updated model of Ria de Aveiro comprises 25 functional groups,
including detritus, phytoplankton, zooplankton, gastropods, annelids,
cephalopods, Manila clams, other bivalves (mainly R. decussatus and
Venerupis corrugata), mysidacea, crustaceans and sh. In this model, the
functional groups of suspended particulate matter, organic matter in the
sediment and halophytes litter were combined into a detritus group, and
the bivalves group was divided into two functional groups: Manila clams
and other bivalves, and on this basis, the ecological carrying capacity of
the Manila clam in the Ria de Aveiro was estimated, and effects of
further increases in clam biomass on other species were investigated.
The input parameters of these functional groups were collected from
various sources, including biomass, catch statistics, empirical relation-
ships, samplings, and experiments studied in other references (Velez
et al., 2015; Bueno-Pardo et al., 2018). Values for P/B (year
−1
), Q/B
(year
−1
) and eet landings (FL, tons km
−2
year
−1
) were based on former
estimates of Bueno-Pardo et al. (2018). The diet composition of the 25
functional groups was introduced as a diet matrix, which can be found in
the reference of Bueno-Pardo et al. (2018).
2.1.2. Ecosim explorations
As a time-dynamic simulation model, Ecosim was used to explore the
potential impacts of different densities of Manila clams on the Ria de
Aveiro ecosystem through both direct and indirect effects. The Ecosim
master equation is as follows:
dBidt =gi
j
Qji −
j
Qji +Ii− (Mi+Fi+ei) × Bi
where dBi/dt represents the growth rate during the time interval dt of
group i in terms of its biomass B
i
, g
i
is the net growth efciency, Q
ji
is the
consumption rates calculated based on the “foraging arena” concept,
where B
i
are divided into vulnerable and invulnerable components
(Walters et al., 1997), I
i
is the immigration rate, M
i
is the nonpredation
natural mortality rate estimated from the EE, F
i
is the shing mortality
rate, and e
i
is the emigration rate.
The vulnerabilities (v) of each functional group in Ecosim, repre-
senting the ows and type of trophic control (i.e., top-down, bottom-up
and mixed control) between predator and prey, were adjusted to be
proportional to the trophic level (Cheung et al., 2002; Christensen and
Walters, 2004; Kluger et al., 2016):
vi=0.1515 ×TLi+0.0485
where TL
i
is the trophic level of a functional group obtained from Eco-
path. The vulnerabilities (v) in Ecomsim range from 0.0 to 1.0, with 0.0
implying a bottom-up control, 1.0 serving as a top-down impact, and 0.3
describing a mixed effect.
The actual vulnerabilities (v
new
) used in the computations range from
1.0 to Inf (Kluger et al., 2016) (Table 1):
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
3
ln(vnew) = 2.301985 ×vi+0.001051
2.1.3. Simulation scenarios
Clam density expansion was simulated for a period of 20 years under
three scenarios with different biomasses of R. philippinarum. The current
status (biomass levels of 154.44 tons km
−2
) of the Ria de Aveiro Ecopath
model was set as Scenario 1 (Bueno-Pardo et al., 2018). Scenarios 2 and
3 were set based on one and two times the ecological carrying capacity
biomass of this species as calculated by Ecopath, respectively. The
biomass of Manila clams chosen for Scenario 3 was one that exceeded
the level of ECC. Scenario 4 was carried out based on 8 times the ECC of
this bivalve species, and the ecosystem collapsed directly. This was the
tipping point where the system collapsed outright. For all three sce-
narios, the following ecological network analysis indicators were used to
describe the responses of the Ria de Aveiro ecosystem to the increase in
Manila clam density: 1) total system throughput, which describes the
sum of all ows through the ecosystem and is identied as the “size of
the ecosystem”; 2) capacity is the product of total system throughput
and entropy and represents the upper limit to ascendency; 3) ascen-
dency, which is the product of growth and development of the system; 4)
Finn cycling index quanties the relative amount of cycling in the sys-
tem and is an indicator of stress, stability and structural differences; 5)
average mutual information is a measure of the information regarding
the network of material exchange within the system; 6) entropy de-
scribes the total number and diversity of ows in a system; 7) transfer
efciency is calculated as the ratio between the sum of the exports plus
the ow transferred from one trophic level to the next and the
throughput on the trophic level; and 8) Kempton’s Q is a relative index
of biomass diversity.
2.2. Physiological measurement
2.2.1. Animal collection and acclimation
Healthy R. philippinarum specimens of three different sizes (Table S1)
were collected from Ria de Aveiro, Portugal, in October 2018. After
sampling, the clams were then transported to the laboratory, where they
were acclimated for seven days in seawater (salinity, 30 ±1; pH, 8.1 ±
0.1) under continuous aeration, a constant temperature of 18.0 ±1.0 ◦C
and a photoperiod of 12:12 h (light/dark). Animals were fed daily with
Algamac Protein Plus during the period of acclimation.
2.2.2. Clearance and egestion rates
The clearance rate was measured by a ow-through system consist-
ing of 12 feeding chambers with square edges (after Rastrick et al., 2018;
Jiang et al., 2021). These chambers were supplied with the same
running seawater as in the acclimation tanks. Nine chambers were used
for individual clams, and three were left empty as controls. Seawater
was pumped to a header tank and through the feeding chambers at a
manually regulated ow rate (average: 207 mL min
−1
). Prior to the
measurements, clams were taken from the laboratory maintenance tank
and acclimated in the feeding chambers for at least 1 h. Water samples
from the outow of both control chambers and chambers with clams
were collected simultaneously. The content of particulate organic matter
(POM) (representing food concentration) was detected by collecting
700 mL seawater from each chamber and ltering through pre-
combusted (450 ◦C, 4 h) and preweighed Whatman GF/C glass micro-
ber lters. Filters were dried to determine dry weight (60 ◦C, 24 h) and
ash free-dry weight (450 ◦C, 4 h) to establish the content of POM. The
clearance rate (CR) of the clam was calculated using the following
formula:
CR L g−1h−1= (Q× (C1– C0)/C1)W
where Q is the ow rate (L h
−1
), C
1
is the outow concentration rep-
resented by the POM in the control (mg L
−1
), C
0
is the outow con-
centration from each experimental chamber (mg L
−1
), and W is the dry
weight of soft tissue (g) (60 ◦C, 48 h).
Clearance rates were converted to ingestion rates of particulate
carbon (POC) of the clam (mg POC g
−1
h
−1
) using the mean temporal
POC content across different seawater layers of the Aveiro coastal
shallow lagoon (Cunha et al., 2003). The ingestion rates of particulate
nitrogen (PON) (mg PON g
−1
h
−1
) were evaluated using POC values and
a Redeld ratio of 6.625 (Redeld, 1934).
The egestion rate of the clam was estimated by using an assimilation
efciency of 0.75 in accordance with van der Veer et al. (2006), which
seems to be reasonable for clams based on ndings from several bivalve
growth models where this estimate produced realistic weights (Pouv-
reau et al., 2006; Filgueira et al., 2011).
2.2.3. Respiration and excretion rates
The respiration rate of nine clams was determined using stop-ow
respirometers (volume 370 mL). The respirometers were supplied with
fully oxygenated ltered seawater. Individuals of R. philippinarum were
placed into a respirometer and allowed to settle to the experimental
conditions for 1 h. At the end of the experiment, the concentration of
dissolved oxygen in each respirometer was kept at a relatively high level
of no less than 60% of the initial dissolved oxygen concentration (based
on a preliminary experiment) to avoid a negative effect on normal
physiological activities. Dissolved oxygen was measured with a Lab-
Quest® 2 multimeter (Vernier, Beaverton, USA). The oxygen con-
sumption rate was detected by the difference between the experimental
and control (without clams) respirometers. The respiration rate (RR) of
the clam was calculated using the following formula:
RR (mg C g
−1
h
−1
) =RQ ×(12/32) ×(DO
c
– DO
e
) ×V/(W ×t)
where RQ is the respiration quotient of 0.85 (Bott, 2006), DO
c
and DO
e
are the dissolved oxygen contents (mg L
−1
) of the control and experi-
mental respirometers, respectively, V is the respirometer volume (L), W
is the dry weight of soft tissue (g) (60 ◦C, 48 h), and t is the measuring
time (h). The experiment lasted for 1 h and the dissolved oxygen con-
centrations in the control and experimental groups were measured
simultaneously at the end of the experiment.
Clam excretion rates, primarily composed of ammonia-N, were
calculated based on stoichiometry (Mayzaud and Conover, 1988) using
a ratio of respiration to excretion for clams of 7.83 obtained by Murphy
et al. (2016).
Table 1
Vulnerabilities for Ria de Aveiro Ecopath model.
Functional group Vulnerabilities (v
i
) Actual vulnerabilities (v
new
)
1 Filter-feeding birds 0.496960453 3.142587507
2 Waders 0.525989671 3.359766010
3 Piscivorous birds 0.598294712 3.968215322
4 Sardine 0.457550000 2.870035034
5 Smelts 0.507212003 3.217631155
6 Seabass 0.528838780 3.381873811
7 Detritivorous sh 0.421626320 2.642243757
8 Zooplanktivorous sh 0.510995564 3.245778157
9 Omnivorous sh 0.518056070 3.298963414
10 Piscivorous sh 0.609390572 4.070879038
11 Zoobenthivorous sh 0.514900174 3.275083863
12 Crustaceans 0.356137718 2.272486678
13 Mysidacea 0.366803015 2.328969834
14 Decapods 0.397248455 2.498051392
15 Manila clams 0.351500000 2.248354752
16 Other bivalves 0.351500000 2.248354752
17 Cephalopods 0.530401351 3.394060366
18 Annelids 0.393278398 2.475325672
19 Gastropods 0.351500000 2.248354752
20 Zooplankton 0.351500000 2.248354752
21 Seagrass 0.200000000 1.586369386
22 Halophytes 0.200000000 1.586369386
23 Phytoplankton 0.200000000 1.586369386
24 Microphytobenthos 0.200000000 1.586369386
25 Detritus 0.200000000 1.586369386
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
4
2.3. Statistical analysis
Statistical analysis was performed using SPSS Statistics (ver. 16.0,
SPSS Inc., Chicago, USA). All data are presented as the mean ±standard
deviation and subjected to analysis of variance (ANOVA) followed by
Duncan’s multiple range test. All differences were considered signicant
at P <0.05.
3. Results
3.1. Ecological carrying capacity and maximum sustained yield
estimation
One target of this study was to determine the ECC and MSY of
R. philippinarum in the marine ecosystem of the Portuguese lagoon. The
Manila clam biomass was 154.44 tons km
−2
and could be increased to
172.40 tons km
−2
, after which the Ecopath model was not balanced, as
the EE for microphytobenthos was >1 (Table 2). Interestingly, the model
parameters estimated for other groups were not affected by this level of
clam biomass except for the EE for phytoplankton, microphytobenthos
and detritus. Therefore, the mass-balance ecosystem model suggested
that the Ria de Aveiro could support a mean R. philippinarum biomass of
172.40 tons km
−2
without signicantly changing the ows of other
functional groups within the system, and this value could be identied
as an estimation of the ecological carrying capacity, which was equiv-
alent to total biomass of 14309 tons of Manila clams. Furthermore, the
maximum sustained yield of these clams was 86.20 tons km
−2
year
−1
,
chosen to be half of the ECC. Increasing the biomass level of this species
to ecological carrying capacity increased total system throughput and
gross efciency, while decreasing net system production and total pri-
mary production/total respiration (Table 3). Furthermore, when the
biomass level of Manila clams surpassed the ECC in the Ria de Aveiro,
net system production and total biomass/total throughput decreased
signicantly.
3.2. Ecological network analyses under different scenarios of Manila clam
biomass
The size of the ecosystem increased due to the increase in Manila
clam biomass from scenarios 1 to 3, which can be seen from the elevated
values of the total system throughput, capacity, and ascendency (Fig. 1).
The Finn cycling index and ascendency increased dramatically due to
the introduction of large clam biomass quantities. The network of ma-
terial exchange, as indicated by average mutual information, decreased
during the rst two years of simulation in scenario 3 and increased
volatility thereafter, with values higher than the initial values for sce-
narios 1 and 2. Rapid increases in transfer efciency were observed in
the three scenarios during the rst year, and then the values decreased.
Interestingly, the value of transfer efciency in scenarios 1 were higher
than that in scenario 3. Changing the R. philippinarum biomass to ECC
resulted in an increase in the total system biomass and caused changes in
the model outputs of the other groups (Fig. 2). The expansion of this
species caused a decrease in the biomass of clam prey (such as phyto-
plankton and microphytobenthos), but an increase in the biomass of
detritus.
3.3. Physiological activities
Figs. 3 and 4 show the physiological rates (ingestion, respiration,
excretion and egestion) of three different clam sizes. Nine individuals
were used for each size category. Physiological rates of R. philippinarum
did not vary signicantly with body sizes. Clearance rates of clams
ranged from 0.51 to 1.16 L g
−1
h
−1
, with a mean value of 0.76 L g
−1
h
−1
(Fig. 3A). R. philippinarum in the small size group (mean shell length,
3.85 ±0.46 cm) had a signicantly higher clearance rate than those in
the medium size group (mean shell length, 4.69 ±0.19 cm) and the
large size group (mean shell length, 5.31 ±0.26 cm) (P <0.05). Similar
to the clearance rate, the average ingestion rates of POC and PON of
clams were 5.22 mg POC g
−1
h
−1
and 0.79 mg PON g
−1
h
−1
(Fig. 3B-C).
Moreover, the egested POC rate ranged from 0.88 mg POC g
−1
h
−1
in the
larger size group and 2.00 mg POC g
−1
h
−1
in the small size group, with
an average rate of 1.30 mg POC g
−1
h
−1
; the egested rate of PON ranged
from 0.13 to 0.30 mg PON g
−1
h
−1
, with a mean value of 0.20 mg PON
g
−1
h
−1
(Fig. 4).
Respiration rates ranged from 0.11 to 0.16 mg carbon (C) g
−1
h
−1
,
with an average value of 0.15 mg C g
−1
h
−1
(Fig. 5A). In the small size
and large size groups, signicantly higher respiration rates were
observed compared with those of the medium size group (P <0.01).
Similarly, the excretion rate ranged from 0.01 to 0.02 mg nitrogen (N)
g
−1
h
−1
, with an average value of 0.02 mg N g
−1
h
−1
(Fig. 5B). No sig-
nicant difference was detected between the small size and large size
Table 2
Changes in Ecopath mode of the Ria de Aveiro when estimating ecological
carrying capacity of Manila clam, Ruditapes philippinarum.
Multiplier Biomass (tons
km
−2
)
Mass-balance changes in model
1.0 (Current condition) 154.44 Balances
Ecological carrying
capacity
1.1 169.89 Balances
1.116291116 172.40 Balances
1.116355866 172.41 Microphytobenthos EE =
1.000028
Notes: EE means ecotrophic efciency.
Table 3
Ecological indices of Ria de Aveiro under different scenarios.
Scenario 1
(Current
condition)
Scenario 2
(Ecological
carrying
capacity)
Scenario 3
(Ecological
carrying
capacity*2)
Units
Sum of all
consumption
8277.04 8547.04 11133.04 tons
km
−2
year
−1
Sum of all
respiratory
ows
4713.62 4858.70 6248.24 tons
km
−2
year
−1
Sum of all ows
into detritus
12386.19 12349.82 12001.39 tons
km
−2
year
−1
Total system
throughput
24043.40 24306.73 26828.76 tons
km
−2
year
−1
Sum of all
production
12539.56 12556.48 12718.53 tons
km
−2
year
−1
Mean trophic
level of the
catch
2.17 2.17 2.12
Gross efciency
(catch/net p.
p.)
0.40 0.50 0.60 %
Total p.p./total
respiration
2.462 2.39 1.86
Net system
production
6891.41 6746.33 5356.79 tons
km
−2
year
−1
Totalp.p./total
biomass
0.86 0.86 0.85
Total biomass/
total
throughput
0.56 0.55 0.51 year
−1
Total biomass
(excluding
detritus)
13439.76 13457.76 13630.16 tons
km
−2
Notes: p.p. means primary production.
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
5
groups (P ≥0.05).
3.4. Carbon and nitrogen budget
When the Manila clam biomass reached the ECC, the annual uxes of
C and N associated with clams in the Ria de Aveiro are shown in Fig. 6.
Of the POC and PON ingested by the Manila clam, 75% was assimilated
and 25% was egested as feces or pseudofeces into the sediments. Sub-
sequently, approximately 3.8%–3.1% of assimilated POC and PON are
respired and excreted by Manila clams. If the harvest biomass for
R. philippinarum was the value of maximum sustained yield (i.e., 86.20
tons km
−2
year
−1
), the annual harvest would account for 581 tons C
year
−1
and 83 tons N year
−1
, respectively, and within this, approxi-
mately 467 tons C year
−1
and 23 tons N year
−1
would be stored in the
clam shells. Respiration and excretion were calculated based on the
monitored physiological activity of Manila clams, and calcication,
mineralization, harvest, denitrication and sedimentation were calcu-
lated based on Mistri and Munari (2012), Murphy et al. (2016), Tang
et al. (2011) and Zhou et al. (2002).
4. Discussion
Here, a food-web Ecopath model was used to determine the
ecological carrying capacity for studying the potential ecosystemic ef-
fects of a further increase in clam biomass on other species groups. The
ECC was calculated following the method of EE (>1) from the Ecopath
model used by many researchers (Jiang and Gibbs, 2005; Byron et al.,
2011a, 2011b). For example, Jiang and Gibbs (2005) predicted the
Fig. 1. Time series of ecological network analysis indices over the 20 years simulation for scenarios 1–3. Scenario 1: the current, scenario 2: one time the ecological
carrying capacity, and scenario 3: two times the ecological carrying capacity of the biomass of Manila clam, Ruditapes philippinarum.
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
6
production and ecological carrying capacity of bivalve shellsh culture
(corresponding to a biomass level of 65 tons km
−2
) in the Golden and
Tasman Bays, and Byron et al. (2011a) calculated the ECC of oyster
culture (corresponding to a biomass level of 297 tons km
−2
) using mass
balance modeling in Narragansett Bay. Our study suggested that the
current biomass level of Manila clams in the Ria de Aveiro of 154.44 tons
km
−2
could be increased to 172.40 tons km
−2
without exceeding the
ecological carrying capacity. Although the estimated carrying capacity
exceeds that found in the Golden and Tasman Bays (comparatively
oligotrophic areas) (Jiang and Gibbs, 2005), it is similar to the level of
the Seine Estuary, with similar characteristics of shallow water depth
and high primary production (Rybarczyk and Elkam, 2003).
Accordingly, the maximum sustained yield of Manila clams is esti-
mated to be 86.20 tons km
−2
year
−1
, and at that point, the clam growth
rate is high (Mace, 2001). Bueno-Pardo et al. (2018) reported that the
current artisanal eet and leisure landings (only referring to legal
catching) of bivalves in the Ria de Aveiro were 33.63 tons km
−2
year
−1
,
much lower than the estimated MSY, suggesting that levels of shing
could increase while remaining sustainable.
A further increase in R. philippinarum has impacts on the ecosystem of
the Portuguese coastal shallow lagoon, as demonstrated by various
ecological indicators, such as total system throughput, ascendency, Finn
cycling index, Kempton’s Q, and transfer efciency (Fig. 1). From sce-
narios 1 to 2, the total system throughput, representing the system’s size
and energy ow (Hermosillo-Nú˜
nez et al., 2018), increased dramati-
cally, and consequently, the elevated ascendency was observed,
improving the systems’ resistance to disturbances. Mature systems have
been reported to have higher values in cycling (Odum, 1969; Kluger
et al., 2016), and thus, the increase in Manila clam biomass up to 172.40
tons km
−2
would lead to an increase in system maturity and stability.
Similarly, the increase in Manila clam biomass to ECC also indicates a
more developed, mature and healthy system. However, a further in-
crease in biomass to the level of scenario 3 had a negative effect on the
biodiversity and health of the ecosystem, as shown by decreases in the
indicators of Kempton’s Q. Moreover, an increasing level of this species
causes a decrease in transfer efciency, suggesting a less efcient
transport of energy between different trophic levels and more energy
being stored in detritus. If clam biomass continued expanding to 8 times
the ecological capacity, it would eventually lead to the collapse of the
Ria de Aveiro ecosystem (biomass of each functional group trends to-
ward 0 with increasing simulation time; data not shown). Furthermore,
the current and ECC states of the ecosystem in the following 20 years
Fig. 2. Biomass levels of several functional groups over the 20 years simulation for scenarios 1–3. Scenario 1: the current , scenario 2: one time the ecological
carrying capacity and scenario 3: two times the ecological carrying capacity of the biomass of Manila clam, Ruditapes philippinarum.
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
7
were compared using Ecosim models. As a major food source for bivalve
mollusks, phytoplankton species are an important limiting factor for the
biomass of clams; however, in the three scenarios evaluated, phyto-
plankton biomass was found to never be below 30% of the original
value. It is possible that the v
new
value of clams used for the simulations
was constant (i.e., 2.25), thereby limiting the increase in feeding pres-
sure on phytoplankton, and it may also be related to the relatively low
value of EE (i.e., ~0.22), indicating the potential growth of the bivalve
lter feeders without exhausting the phytoplankton (Kluger et al.,
2016).
The increase in clam biomass has a top-down control on its prey, such
as, phytoplankton and microphytobenthos, thereby decreasing the bio-
masses of these groups. However, interestingly, as the major competitors
with bivalves for food, the zooplankton group was impacted only
slightly during the simulations (Fig. 2). Here, zooplankton are mainly
preyed upon by small shes, such as sardine and zooplanktivorous sh.
The increase in clams may lead to a decrease in the biomass of small sh
groups through the increase in carnivorous sh, thereby reducing the
predation pressure on the zooplankton (Kluger et al., 2016). This result
is quite different from the studies of Jiang and Gibbs (2005) and Byron
et al. (2011a), who assumed that bivalve would replace zooplankton in
the system.
Bivalve lter feeders perform a suite of ecosystem services. By
ltering phytoplankton, bivalves increase water transparency and may
help prevent the occurrence of harmful algal blooms. In the Ria de
Aveiro, clam clearance rates ranged from 0.51 to 1.16 L g
−1
h
−1
, with a
Fig. 3. Clearance rate (A), ingestion rate of particulate carbon (POC) (B) and particulate nitrogen (PON) (C) measurements of different sizes of Manila clam,
Ruditapes philippinarum. Bars with different letters are statistically different (P <0.05).
Fig. 4. Egestion rate of particulate carbon (POC) (A) and particulate nitrogen (PON) (B) measurements of different sizes of Manila clam, Ruditapes philippinarum. Bars
with different letters are statistically different (P <0.05).
Fig. 5. Respiration rate (A) and excretion rate (B) measurements of different sizes of Manila clam, Ruditapes philippinarum. Bars with different letters are statistically
different (P <0.05).
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
8
mean value of 0.76 L g
−1
h
−1
(Fig. 3A). With this ltering capacity, the
number of days required by the bivalve community (reaching its
ecological carrying capacity) to lter the entire seawater of the Ria de
Aveiro was approximately 7 days. Dame and Prins (1998) and Murphy
et al. (2016) reported that the bivalve population would control the
phytoplankton if the time taken by them to lter the entire system was
shorter than the turnover time of phytoplankton/primary production
and the residence time of water mass. Here, Ria de Aveiro has relatively
shorter phytoplankton turnover times (~1.7 days) (Bueno-Pardo et al.,
2018; Frankenbach et al., 2020) and greatly varied system residence
times (0–15 days) (Dias et al., 2007), implying that it might support the
ecological carrying capacity of clams associated with a rapid clearance
time (~7 days). Interestingly, in this study, small clams showed the
highest clearance rate and medium and large clams had similar lower
rates, perhaps due to small individuals growing faster than large ones.
Small clams were more active in feeding to meet their high growth rates
and nutritional requirements. This is consistent with results from other
bivalve species, such as the Iwagaki oyster Crassostrea nippona (Wang
and Li, 2020) and the pearl oyster Pinctada margaritifera (Yukihira et al.,
1998). Moreover, large clams had higher respiration and excretion rates
than medium ones. It is possible that large clams become sexually
mature at a dry esh weight of about 1.6 g, and at that stage, more
energy is required for both growth and gamete production.
Bivalves have also been suggested as an indirect way to control
eutrophication by extracting nutrients, called “nutrient bioextraction”
(Bricker et al., 2014; Murphy et al., 2016). Some researchers have
argued that this removal of nutrients should be assessed based on the
harvest and regenerated N of bivalves to analyze the net impacts of
bivalve activities on ecosystems (Nizzoli et al., 2005, 2011; Murphy
et al., 2016). However, others pointed out that the nutrients recovered in
the sediments associated with biodeposition by bivalve farming ulti-
mately come from primary production in the ecosystem and remain
locked within the sediment (Stadmark and Conley, 2011). In the Ria de
Aveiro, approximately 83 tons N year
−1
would be removed from the
ecosystem through clam harvesting (when it reached the maximum
sustained yield), which was similar to results reported by Stadmark and
Conley (2011). PON was ingested by bivalves and egested as feces and
pseudofeces. These biodeposits could be decomposed by the bacteria
and further produce nitrogen gas through the processes of mineraliza-
tion, nitrication and denitrication, which is also an important way to
remove N. Here, approximately 2 tons year
−1
would be removed
through denitrication annually (calculated from Murphy et al., 2016).
Furthermore, bivalves can signicantly alter carbon uxes in marine
ecosystems, leading to carbon sequestration or storage. Bivalves convert
the dissolved CO
2
into their CaCO
3
shells. This shell material can pro-
vide a long-term carbon sink and is considered a way to offset the
increasing carbon in the atmosphere (Emery, 2015; Murphy et al.,
2016). Here, our study of the Portuguese population of Manila clams
suggests that harvested clams of the maximum sustained yield represent
the removal of ~7 g carbon m
−2
year
−1
(Fig. 6). As described earlier, the
overall effect of bivalves on the carbon cycle is still controversial, as they
can produce CO
2
during their own metabolic processes, similar to other
animals. However, researchers recently reported that the CO
2
released
by bivalves could support the photosynthesis of phytoplankton or
macroalgae and could exclusively be recycled in marine ecosystems
(Jiang et al., 2015). In many large-scale shellsh mariculture areas, such
as Sanggou Bay, the annual uptake of dissolved inorganic carbon was up
to 1.39 ×10
5
tons, indicating their high capacities of CO
2
absorption
(Jiang et al., 2015). Therefore, an integrated ecosystem approach is
needed to further investigate the complex role of bivalves in the carbon
cycle and to understand the ecosystems’ goods and services of bivalves
(Filgueira et al., 2011).
5. Conclusion
The developed Ecopath model successfully estimated the ecological
carrying capacity (i.e., 172.40 tons km
−2
) and maximum sustained yield
(i.e., 86.20 tons km
−2
year
−1
) of the Manila clam, R. philippinarum in Ria
de Aveiro. Indeed, the harvested Manila clams with the MSY represent
the removal of ~581 tons C and ~83 tons N annually, with substantial
ecological and economic implications. Simulations of a further biomass
of this species increase suggest that exceeding the biomass level of
172.40 tons km
−2
may cause the EE of other groups to become unreal-
istic, potentially leading to decreases in the ecosystem transfer ef-
ciency, biodiversity, and health. The results can be used to guide the
sustainable management of bivalves in theRia de Aveiro and the pro-
tection of the local environment.
Funding
The research was supported by the Natural Science Foundation of
Shandong Province (ZR2021QD035), Key Programme for International
Cooperation on Scientic and Technological Innovation, Ministry of
Science and Technology (2017YFE0118300), National Natural Science
Foundation of China (41761134052), Central Public-interest Scientic
Fig. 6. Annual uxes of carbon (A) and nitrogen (B) associated with bivalve
lter feeders in the Ria de Aveiro. Calcication, mineralization, harvest, deni-
trication and sedimentation were calculated based on Mistri and Munari
(2012), Murphy et al. (2016), Tang et al. (2011) and Zhou et al. (2002).
Abbreviation: MSY, maximum sustained yield; DIC, dissolved inorganic carbon;
DIN, dissolved inorganic nitrogen.
W. Jiang et al.

Marine Environmental Research 190 (2023) 106117
9
Institution Basal Research Fund, CAFS (2020TD50), Young Taishan
Scholars Program of Shandong Province (tsqn201909166), and China
Agriculture Research System of MOF and MARA. This work was also
nancially supported by the project ASARISAFE–Safety and sustainable
management of valuable clam product in Portugal and China funded by
the National Funds through the Portuguese Science Foundation (FCT).
Francesca Coppola beneted from a PhD grant (SFRH/BD/118582/
2016) given by FCT, supported by FSE and Programa Operational
Capital Humano (POCH) e da Uni˜
ao Europeia. Thanks are also due for
the nancial support of CESAM (UIDP/50017/2020+UIDB/50017/
2020+LA/P/0094/2020).
Authors’ contributions
Weiwei Jiang: Conceptualization, Methodology, Writing - original
draft, Writing - review & editing, Funding acquisition. Francesca Cop-
pola: Investigation, Data curation, formal analysis, Writing - review &
editing. Zengjie Jiang, Rosa Freitas and Yuze Mao: Methodology,
Writing - review & editing, Funding acquisition. Zhijun Tan, Jinghui
Fang, Jianguang Fang and Yitao Zhang: Investigation, Formal analysis,
Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Data availability
Data will be made available on request.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.marenvres.2023.106117.
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