J Appl Phycol (2016) 28:3083–3089
DOI 10.1007/s10811-016-0858-8
A comparative study of the nutrient uptake and growth capacities
of seaweeds Caulerpa lentillifera and Gracilaria lichenoides
Hengtong Liu 1,2 & Fang Wang 1,2 & Qiaohan Wang 1,2 & Shuanglin Dong 1,2 & Xiangli Tian 1,2
Received: 3 February 2016 / Revised and accepted: 9 April 2016 / Published online: 19 April 2016
# Springer Science+Business Media Dordrecht 2016
Abstract Intensive fish aquaculture activities release large
amount of nitrogen (NH4-N and NO3-N) to the surrounding
waters and lead to water eutrophication. However, integrating
a single species of seaweed with the fed fish usually cannot
remove both forms of nitrogen efficiently. Polyculture of dif-
ferent seaweeds will be an effective way to reduce the nitrogen
load of surrounding waters. To compare the feasibility of
using Caulerpa lentillifera and Gracilaria lichenoides as
biofilters to treat marine fish aquaculture effluents, nine
NH4-N/NO3-N ratios were set up and the nitrogen uptake
and growth rate of the two seaweeds were measured. The
main results showed that: (1) In the presence of multiple
N sources, C. lentillifera selectively takes up NO3-N prior to
NH4-N and the NO3-N uptake rate was 7.43–50.43 μmol g−1
(dw) h −1 which was significantly higher than that of
G. lichenoides. Gracilaria lichenoides selectively takes up
NH4-N prior to NO3-N and the NH4-N uptake rate was
10.27–14.14 μmol g−1 (dw) h−1 which was significantly
higher than that of C. lentillifera. (2) The NH4-N/NO3-N ratio
had effects on the growth of the two seaweeds: 1/1 and 1/5 of
NH 4 -N/NO 3 -N were favorable for the growth of
C. lentillifera; 1/4 and 1/0.5 of NH4-N/NO3-N were favorable
* Fang Wang
wangfang249@ouc.edu.cn
* Qiaohan Wang
wangqiaohan@ouc.edu.cn
1
Key Laboratory of Mariculture, Ministry of Education, Ocean
University of China, Qingdao 266003, China
2
Function Laboratory for Marine Fisheries Science and Food
Production Processes, Qingdao National Laboratory for Marine
Science and Technology, No. 1 Wenhai Road, Aoshanwei Town,
Jimo, Qingdao 266237, China
for the growth of G. lichenoides. The results preliminarily
indicate that integrated culture of C. lentillifera and
G. lichenoides was sufficient for bioremediation of marine
fish aquaculture effluents.
Keywords Chlorophyta . Rhodophyta . Ammonium .
Nitrate . Uptake rate . Growth
Introduction
In terms of the growing shortage of water and space, industrial
aquaculture has become one of the most sustainable models to
culture fish. Because high density of fish is cultured with
limited volumes of water, effluents from an industrial aqua-
culture system usually contain high concentration of nutrients,
which poses a potential risk to the surrounding environment
(Piedrahita 2003). Bioremediation technology has been devel-
oped to treat aquaculture effluents from industrial aquaculture.
Bioremediation of aquaculture effluents mainly includes
microorganism dissimilation or assimilation (Burgin et al.
2011; Castine et al. 2013), micro- and macro-algae for photo-
tropic plant nutrient uptake (Neori et al. 1996; Metaxa et al.
2006), and constructed wetland units (Sikora et al. 1995; Lin
et al. 2003). Because of low cost and high uptake efficiency,
seaweeds have become a potentially feasible alternative in the
bioremediation of effluents (Chopin et al. 2001; Neori et al.
2004). Several seaweeds such as Ulva lactuca L. and Undaria
pinnatifida Suringar (Cahill et al. 2010), Gracilaria birdiae
E.M. Plastino & E.C. Oliveira (Matos et al. 2006; Marinho-
Soriano et al. 2009), and Pyropia leucosticta (Thuret) Neefus
& Brodie (Chung et al. 2002) are usually used as biofilters to
treat aquaculture effluents. However, these seaweeds mainly
take up NH4-N as N source. Neori et al. (2004) showed that
the percentage of NO3-N was usually higher than NH4-N in
3084
aquaculture effluents. Therefore, polyculture of a NO3-N fa-
voring seaweed with a NH4-N favoring seaweed will be an
efficient strategy to remove nitrogen from aquaculture efflu-
ents. Previous studies on the polyculture of seaweeds showed
that seaweed niche partitioning and diversity dramatically en-
hanced nitrogen uptake via complementary use of nitrate and
ammonium (Bracken and Stachowicz 2006), as well as sea-
weed biomass (Stachowicz et al. 2008).
Caulerpa lentillifera J. Agardh is a green alga with high
economic value and is naturally distributed in tropical regions
(Paul et al. 2014). It is considered as an important source of
polyunsaturated fatty acids (PUFA) and has been shown to be
effective in removing basic dyes from waste streams
(Marungrueng and Pavasant 2006) and heavy metals from
industrial wastewater (Pavasant et al. 2006; Apiratikul and
Pavasant 2008). Furthermore, C. lentillifera has significant
uptake capacity for nutrients (Paul and De Nys 2008), espe-
cially NO3-N (Guo et al. 2015). Previous studies have gener-
ally not on nutrient uptake and growth of C. lentillifera in the
presence of multiple N sources. Tilman et al. (1996) and
Hooper et al. (2005) also observed that biodiversity might
enhance the management of nutrient uptake and storage, but
this suggestion has been controversial, in part because the
specific biological mechanisms by which species diversity
influences nutrient uptake have not been identified (Loreau
et al. 2001). As a result, a comparative study between
C. lentillifera and conventional biofilter seaweed Gracilaria
lichenoides (J.V. Lamouroux) Greville is of importance, as
well as the polyculture of the two seaweeds in the treatment
of aquaculture effluents.
In the present study, nine NH4-N/NO3-N ratios were set up
to compare the differences of nitrogen uptake and growth
capacities between C. lentillifera and G. lichenoides. We ex-
pect to answer the following two questions: (1) will
C. lentillifera and G. lichenoides selectively take up N from
two sources (NH4-N and NO3-N)? (2) What are the differ-
ences of nitrogen uptake and growth capacities between
C. lentillifera and G. lichenoides? The main results of the
study are expected to supply a scientific reference for efficient
nitrogen removal from aquaculture effluents.
Materials and methods
Source and pre-culture of the seaweeds
Caulerpa lentillifera and Gracilaria lichenoides were collect-
ed from algae farm in Hainan, China (19° 10′ N, 109° 43′ E) in
July 2014. After collection, the seaweeds were transferred to
the laboratory and then cleaned of epiphytes and encrusting
organisms with autoclaved seawater. Afterwards, they were
placed in an illuminating incubator (GXZ Series, Jiangnan,
China) and pre-cultured for 7 days until the start of the
J Appl Phycol (2016) 28:3083–3089
experiments. The seawater used for pre-culture was collected
from the coastal waters of Qingdao, China, and the salinity
was 29 psu. Seawater was replaced once a day during the pre-
culture period. The pre-culture was conducted under con-
trolled conditions of photon flux density (90 μmol photons
m−2 s−1), temperature (25 ± 0.5 °C), and photoperiod (14:10;
light:dark) and the culture was continuously aerated.
Preparation of N-removed seawater
One hundred fifty liters of seawater was placed into four
aquaria (50 cm × 75 cm × 45 cm) and a total of 300 g
G. lichenoides was placed in each to remove the possible
nutrient. Water was continuously aerated. During this period,
nutrient concentrations (NH4-N, NO3-N, and PO4-P) were
monitored every 12 h. When the inorganic nitrogen in the
seawater decreased to a negligible 0.04 mg L−1 (inorganic
phosphorus decreased to 0.01 mg L−1), the seawater could
be considered as N-removed water which would be used for
the preparation of culture medium. The preparation of the N-
removed seawater was done on multiple occasions and oc-
curred within 36–48 h.
Nutrient uptake experiment
The experiment was carried out inside an illuminating incu-
bator and lasted for 10 h. Throughout this experiment, all the
cultures were kept at the same conditions of temperature, pho-
ton flux density, and photoperiod mentioned in BSource and
pre-culture of the seaweeds.^ The NH4-N/NO3-N ratios of the
nine treatments are described in Table 1. Three replicates were
used for each experimental treatment and three algae-free
flasks were used as controls. The culture medium was pre-
pared with N-removed seawater (mentioned in BPreparation
of N-removed seawater^) which was then enriched with var-
ious initial nutrients concentrations from stock solution of
NH4Cl, NaNO3, and NaH2PO4 (P was added to keep N/P
equal to 10). The seaweed samples selected after pre-culture
were randomly added to 1 L acid-washed Erlenmeyer flasks
containing 800 mL of the respective culture medium. The
initial seaweed stocking density was 2 g (fw) L−1. Duplicate
6 mL water samples were collected from each flask before
adding seaweeds and after the end of the experiment to deter-
mine the initial and final NH4-N and NO3-N concentrations.
Table 1 The NH4-N/NO3-N and total nitrogen (TN) concentrations
(mg L−1) used to set up the experimental conditions
Treatment 1 2 3 4 5 6 7 8 9
NH4-N/NO3-N 1/0.5 1/1 1/2 1/3 1/4 1/5 1/10 1/15 1/20
TN 1.5 2.0 3.0 4.0 5.0 6.0 11.0 16.0 21.0
J Appl Phycol (2016) 28:3083–3089
At the end of the experiment, seaweed material was cleaned
with N-removed seawater and dried to a constant weight
(48 h) in an oven at 60 °C to determine dry weight (dw).
The nutrient concentrations in the water samples were mea-
sured by Four-Channel Auto Analyzer (QuAAtro, SEAL
Analytical, Germany). Nutrients uptake rates were calculated
following the formula (Pedersen 1994):
. (Fig. 1a). When NH4-N/NO3-N were 1/5 and 1/2, NH4-N
V ¼ ðS 0 *a−St *bÞ ðdw*t Þ
Where V is uptake rate (μmol g−1 (dw) h−1), S0 and St and a
and b are the substrate nutrient concentrations and the water
volume at the beginning and at the end of the experiment, (μM
and mL, respectively), dw is the dried seaweed biomass (g),
and t is the elapsed time between the sampling intervals (h).
Growth experiment
This experiment was designed as in BNutrient uptake
experiment^ and lasted for 15 days. Every 3 days, fresh
weight (fw) of the two species was determined after they
were blotted dry and the culture medium was replaced. At
the end of the experiment, seaweed material was weighed
and dried to a constant weight (48 h) at 60 °C. Dried sam-
ples were ground with a mortar and pestle to homogeneous
powder for analysis of carbon and nitrogen content (% dw)
in the tissue with a CHNSO Analyser (Vario EL III,
Elementar, Germany). The specific growth rates (SGR) for
the total duration of the experiment were calculated follow-
ing the formula (Yong et al. 2013):
  . (Fig. 1b). On the other hand, for G. lichenoides, the rates of
SGR %day−1 ¼ 100*½Lnð f wt Þ−Lnð f w0 Þ t
Where fwt is the final fresh weight (g), fw0 is the initial fresh
weight (g), and t is the time in culture (d).
Statistical analysis
All values are given as mean ± SD. Normal distribution and
homogeneity of variances were tested by the Kolmogorov-
Smirnov and Levene tests, respectively. One-way ANOVA
was used to analyze the responses of C. lentillifera and
G. lichenoides to the different NH4-N/NO3-N conditions in
terms of nutrients uptake rates, biomass, SGR, and tissue C
and N content. Duncan multiple range test was applied to
evaluate differences between significant means. Independent
Samples t test was used to analyze the differences of these
indices mentioned above between C. lentillifera and
G. lichenoides. Analyses had a critical probability level of
0.05. All statistical analyses were performed using the SPSS
Statistics 17.0.
3085
Results
Nutrient uptake
NH4-N uptake The NH4-N uptake rates of C. lentillifera fluc-
tuated with different NH4-N/NO3-N ratios in the medium with
no significant difference among nine treatments (P > 0.05)
uptake rates by C. lentillifera obtained the maximum and min-
imum values, 7.67 ± 0.68 and 5.69 ± 0.72 μmol g−1 (dw) h−1,
respectively. The NH4-N uptake rates of G. lichenoides varied
significantly with different NH4-N/NO3-N ratio (P < 0.05),
which indicated that NH4-N/NO3-N in the medium had a sig-
nificant effect on the NH4-N uptake capacity of G. lichenoides
(P < 0.05). The G. lichenoides NH4-N uptake rates decreased
with decreasing NH4-N/NO3-N and the maximum and mini-
mum values, 14.14 ± 1.34 and 10.27 ± 0.86 μmol g−1 (dw)
h−1, were observed for G. lichenoides subjected to 1/0.5 and
1/20 of NH4-N/NO3-N, respectively. Of the two species
assayed, G. lichenoides showed markedly higher uptake rates
for NH4-N than C. lentillifera in all the experimental treat-
ments (P < 0.05) (Fig. 1a).
NO3-N uptake As shown in Fig. 1b, minimum uptake rates of
NO3-N (7.43 ± 0.36 μmol g−1 (dw) h−1) for C. lentillifera oc-
curred when NH4-N/NO3-N was 1/0.5 and the uptake rates
significantly increased with decreasing NH4-N/NO3-N. The
maximum rate (50.43 ± 5.93 μmol g−1 (dw) h−1) was observed
when NH4-N/NO3-N was 1/5. With a further decrease in NH4-
N/NO3-N, NO3-N uptake rates for C. lentillifera slightly de-
creased and were stable at 44.99 ± 4.28 μmol g−1 (dw) h−1
NO3-N uptake increased with a decrease in NH4-N/NO3-N.
Maximum NO3-N uptake rate of G. lichenoides (61.12
± 3.66 μmol g−1 (dw) h−1) occurred when NH4-N/NO3-N
was 1/20, which was significantly higher than that of
C. lentillifera at the same NH4-N/NO3-N. While the NO3-N
uptake rates of C. lentillifera were significantly higher than
those of G. lichenoides in the case of substrate NH4-N/NO3-N
in the range of 1/0.5 to 1/10 (P < 0.05) (Fig. 1b).
Growth
Biomass and SGR As shown in Fig. 2a, b, with the decrease
of NH4-N/NO3-N, the biomass and SGR of C. lentillifera first
increased and then decreased. The maximum values of bio-
mass and SGR (3.64 ± 0.05 g and 3.99 ± 0.02 % d−1, respec-
tively) were reached at the NH4-N/NO3-N ratio of 1/4. A
significant escalating trend in the biomass and SGR of
C. lentillifera was observed when NH4-N/NO3-N was approx-
imate to 1/1 (P < 0.05). Correspondingly, biomass and SGR of
G. lichenoides decreased gradually with the decrease in the
NH4-N/NO3-N ratio and the maximum values (3.61 ± 0.08 g
3086
Fig. 1 Uptake rates of NH4-N (a) and NO3-N (b) by C. lentillifera and G. lichenoides. Note: The asterisk represents a significant difference between the
two seaweeds (P < 0.05), data are mean ± SD, n = 3
and 3.94 ± 0.03 % d−1) were recorded when the NH4-N/NO3-
N ratio was the highest. Significant escalating trends in bio-
mass and SGR of G. lichenoides were observed when NH4-N/
NO3-N was approximate to 1/4 (P < 0.05) (Fig. 2a, b).
The biomass of G. lichenoides was higher than
C. lentillifera with the NH4-N/NO3-N ratio in the range of
1/0.5 to 1/3. However, the difference was not significant
except in the group with the highest NH4-N/NO3-N of 1/0.5.
When NH 4 -N/NO 3 -N were 1/4–1/5, the values for
C. lentillifera maintained at the highest level; however, a sig-
nificant reduction in the biomass of G. lichenoides was ob-
served (P < 0.05). With a further decrease in NH4-N/NO3-N
(1/10–1/20), the biomass of G. lichenoides and C. lentillifera
all decreased to a relatively low level and no significant differ-
ence was found between the two species (P > 0.05) (Fig. 2a, b).
Carbon and nitrogen tissue content As shown in Fig. 2c, d,
the C and N content in the tissue of C. lentillifera showed
similar trends as the change of NH4-N/NO3-N and the maxi-
mum values (24.20 ± 1.56 % and 2.22 ± 0.04 %, respectively)
were obtained when NH4-N/NO3-N was 1/2. The C and N
content in the tissue of G. lichenoides increased first and then
decreased with the decrease of NH4-N/NO3-N and the maxi-
mum values of C and N content (30.16 ± 0.43 % and 2.98
± 0.07 %) were obtained at NH4-N/NO3-N of 1/2 and 1/4,
respectively. As shown in Fig. 2e, with the decrease in NH4-
N/NO3-N, the C/N in the tissue of C. lentillifera showed no
significant difference among the nine treatments (P > 0.05) and
the same was found in G. lichenoides. The maximum C/N in
C. lentillifera and G. lichenoides was obtained in the tissue
exposed to NH4-N/NO3-N of 1/2 and 1/0.5, respectively.
Discussion
This study showed that C. lentillifera and G. lichenoides could
assimilate nitrogen even with NH4-N/NO3-N as low as 1/20.
The forms and ratios of the two forms of inorganic nitrogen
J Appl Phycol (2016) 28:3083–3089
(NH4-N and NO3-N) had marked influences on the nutrients
uptake and growth of the two seaweeds.
Under the experimental conditions, there was a significant
difference between the two seaweeds in the selection of the
two N sources. The G. lichenoides was significantly more
efficient in depleting NH4-N than C. lentillifera. Intracellular
nitrogen pools and correlative enzyme activity may be two of
the factors that are responsible for the different affinity for
NH4-N (Thomas and Harrison 1985). With the increase in
medium nitrogen concentrations, the biomass of
G. lichenoides increased correspondingly to the NH4-N up-
take rates, demonstrating that the biomass production of
G. lichenoides was mainly generated from NH4-N assimila-
tion. Selectivity of nutrient uptake has been confirmed in other
N-deprived seaweeds, including Gracilaria tikvahiae
McLachlan (Ryther et al. 1981), Ulva rotundata Bliding
(Hernández et al. 2002), and Ulva intestinalis Linnaeus
(Cohen and Fong 2004). One possible explanation is that uti-
lization of ammonium is more metabolically energy-efficient
than nitrate, because ammonium can be incorporated directly
into amino acids (Lobban and Harrison 1994). It has been
reported that C. lentillifera has a strong affinity for NO3-N
(Pariyawathee et al. 2003; Guo et al. 2015) and this was fur-
ther verified in the present study. Both the biomass and NO3-N
uptake rates of C. lentillifera showed a similar trend with the
decrease in medium NH4-N/NO3-N. This indicated that the
biomass production of C. lentillifera was mainly from NO3-
N assimilation. Previous studies have shown that many sea-
weeds prefer to assimilate NH4-N compared with NO3-N (Ale
et al. 2011; Luo et al. 2012). In the present study, C. lentillifera
was more effective in removing NO3-N than G. lichenoides.
The specific nutrient metabolic regulation system in
C. lentillifera may contribute to NO3-N uptake (Guo et al.
2015). Previous studies have indicated that nitrate reductase
is one of the key enzymes involved in NO3-N uptake and
assimilation. The nitrate reductase in C. lentillifera is more
active than that in G. lichenoides (Nirmal Kumar et al.
2010), which is probably one of the reasons for the significant
J Appl Phycol (2016) 28:3083–3089
Fig. 2 Biomass (a), RGR (b), tissue C content (dw %) (c), tissue N
content (dw %) (d), and total C/N ratios (e) of C. lentillifera and
G. lichenoides cultured under nine experimental treatments. Note: The
difference on the nitrate uptake between the seaweeds. In ad-
dition, Thomas and Harrison (1985) found an inverse correla-
tion between nitrate uptake rate and the storage of intracellular
nitrate pool in Pyropia (Porphyra) perforata and nitrate pool
size directly affected nitrate uptake. In the present study, the
difference in nitrate uptake rate between the seaweeds may be
related to the difference of the intracellular nitrate pool size.
It was reported that the nitrogen content and C/N ratio in
tissue of seaweeds usually reflect the nitrogen restriction from
ambient environment (Neori et al. 1991; Friedlander and Levy
1995). The critical C/N value range of Gracilaria spp. is 10–15
and a value greater than 15 indicated that growth of seaweed
3087
asterisk represents a significant difference between the two seaweeds
(P < 0.05), data are mean ± SD, n = 3
has been limited by ambient nitrogen content, while the value
less than 10 indicated that the seaweed has already started to
store nitrogen (Xu and Zou 2008). The C/N ratios in tissue of
seaweeds in every treatment were all less than 15 in this study,
indicating that the substrate nitrogen concentrations were suf-
ficient. When the NH4-N/NO3-N was relative high (in the
range of 1/0.5 to 1/3), the NH4-N/NO3-N of 1/1 was favorable
for the growth of C. lentillifera. These results also have been
confirmed for Grateloupia turuturu Yamada (Lan 2013).
Nutrient uptake and growth of C. lentillifera were stimulated
under relative low NH4-N/NO3-N (in the range of 1/4 to 1/20).
The maximum NH4-N and NO3-N uptake rates, biomass, and
3088
C/N in the tissue of C. lentillifera were obtained when NH4-N/
NO3-N was 1/5, which were approximate to the results of a
previous study (Pariyawathee et al. 2003). Variations in NH4-
N/NO3-N have an effect on the magnitude of the seaweed
intracellular protein-nitrogen pool and amino acid-nitrogen
pool and proper ratios of N sources contribute to uptake and
utilization of nitrogen (Naldi and Wheeler 1999). This may be
an explanation for the relationship between NO3-N uptake and
growth rates of C. lentillifera under proper NH4-N/NO3-N.
When the NH4-N/NO3-N in the substrate changed, the change
pattern of total N content in tissue of C. lentillifera was not
completely consistent with that of biomass. One possible rea-
son is that the increase of growth rate led to a decrease in the
percentage of N in the tissue due to dilution (Teichberg et al.
2008). The present study also indicated that growth of
G. lichenoides would be enhanced under relative low NH4-N/
NO3-N (in the range of 1/4 to 1/20). The maximum N content
and minimum C/N ratio in the tissue were observed under
NH4-N/NO3-N of 1/4, demonstrating that nitrogen was effi-
ciently assimilated by G. lichenoides. Previous observations
by Huang et al. (2006) showed that SGR, pigments, and protein
content of G. tenuistipitata var. liui C.F. Chang & B.M. Xia rise
to the highest level when the NH4-N/NO3-N ratio in the culture
medium was 2/7, which is similar to the results of the present
study. It was further shown that multiple N sources in appro-
priate ratios were superior to a single N source (NH4-N or NO3-
N) for the growth and protein accumulation in G. lichenoides.
The optimal growth status and highest NH4-N uptake rate was
observed in G. lichenoides when the substrate NH4-N/NO3-N
was 1/0.5, which is similar to the results of previous studies on
G. tenuistipitata var. liui (Xu et al. 2001).
Potential for aquaculture effluents bioremediation
In most industrial aquaculture systems in China, the wastes of
the fed fish release abundant nutrients which pollute the cul-
tivation and surrounding waters (Yang et al. 2015). It has been
shown that integrating fish mariculure systems with seaweeds
significantly reduces the total discharge of dissolved nutrients
to the environment (He et al. 2008; Yang et al. 2015). The
study of Bracken and Stachowicz (2006) showed that when
multiple N sources were present, the polyculture system of
different seaweeds was more effective at removing both
NH4-N and NO3-N, resulting in enhanced total nitrogen up-
take. In the presence of a suitable NH4-N/NO3-N ratio,
C. lentillifera has pronounced uptake and assimilation abilities
for NO3-N and is expected to effectively control water nitrate
concentrations and transfer nitrate to biomass; however, its
removal abilities for NH4-N is lower than G. lichenoides.
Instead, G. lichenoides is able to remove NH4-N efficiently
from effluents, but its uptake performance of nitrate is inferior
to C. lentillifera. In this case, integrated cultivation of
C. lentillifera and G. lichenoides will be an efficient way to
J Appl Phycol (2016) 28:3083–3089
remove NH4-N and NO3-N from aquaculture effluents. In the
middle-scale pond experiment (lasted for 30 days), we
polycultured the C. lentillifera and G. lichenoides in a cement
pond (6 m × 6 m). The C. lentillifera was cultivated in small
cages and the G. lichenoides was cultivated by the floating-
raft method. The experiment indicated that the two seaweeds
could be co-cultured and had a high uptake rate for the nitro-
gen from the effluents of fed fish. However, the stocking den-
sity and co-location of the two seaweeds to obtain the optimal
effect needs furher study.
Acknowledgments We thank all members of Ecology Lab for practical
assistance and technical support. We also thank Dr. L Li for the English
review of this paper. This study was supported by the Major Project for
Agricultural Application Technology Innovation of Shandong Province
(Grant No. 2013–136) and Function Laboratory for Marine Fisheries
Science and Food Production Processes, Qingdao National Laboratory
for Marine Science and Technology.
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