MPB-08235; No of Pages 5

Marine Pollution Bulletin xxx (2016) xxx–xxx

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Ocean acidification: One potential driver of phosphorus eutrophication

Changzi Ge ⁎, Yanchao Chai, Haiqing Wang, Manman Kan
Marine College, Shandong University, Weihai, Weihai 264209, China

a r t i c l e i n f o a b s t r a c t

Article history: Harmful algal blooms which may be limited by phosphorus outbreak increases currently and ocean acidification
Received 29 June 2016 worsens presently, which implies that ocean acidification might lead to phosphorus eutrophication. To verify the
Received in revised form 20 November 2016 hypothesis, oxic sediments were exposed to seawater with different pH 30 days. If pH was 8.1 and 7.7, the total
Accepted 6 December 2016
phosphorus (TP) content in sediments was 1.52 ± 0.50 and 1.29 ± 0.40 mg/g. The inorganic phosphorus (IP)
Available online xxxx
content in sediments exposed to seawater with pH 8.1 and 7.7 was 1.39 ± 0.10 and 1.06 ± 0.20 mg/g, respective-
Keywords:
ly. The exchangeable phosphorus (Ex-P) content in sediments was 4.40 ± 0.45 and 2.82 ± 0.15 μg/g, if seawater
Eutrophication pH was 8.1 and 7.7. Ex-P and IP contents in oxic sediments were reduced by ocean acidification significantly
Exchangeable phosphorus (p b 5%). The reduced phosphorus in sediments diffused into water, which implied that ocean acidification
Inorganic phosphorus was one potential facilitator of phosphorus eutrophication in oxic conditions.
Ocean acidification © 2016 Published by Elsevier Ltd.

1. Introduction
Nutrients eutrophication is one dominant promotive factor for
harmful algal blooms outbreak which results in various ecological
risks (Hart et al., 2015; Zhang et al., 2015). High concentrations of nutri-
ents may lead to eutrophication (Rothenberger and Calomeni, 2016)
and attentions from different interest groups have been focused on
nutrient eutrophication (Yan et al., 2016). Phosphorus concentration
promotion can result in algae multiplication (Wang et al., 1996). Phos-
phorus limitation for primary production of marine becomes generally
because terrigenous phosphorus discharge has been reduced globally
(Chen et al., 2015). Thus, harmful algal blooms may occur with high
possibility if phosphate concentration increases and the relationships
between phosphorus concentration increase and harmful algal blooms
outbreak were confirmed by field experiments (Zhang et al., 2007;
Yamaguchi et al., 2008; Cao et al., 2009; Xia et al., 2009; Song et al.,
2011b; Wang et al., 2011; Gao et al., 2012; Gao et al., 2014). Phosphorus
in water body mainly originates from runoffs, marine organisms excre-
tions and diffusion across sediment-water interface (Hessen et al., 2010;
García-Romero et al., 2014; Han et al., 2015), and the phosphorus diffu-
sion flux across sediment-water interface is influenced by water pH
values (Ni and Wang, 2015; Gainswin et al., 2006). Ocean acidification
refers to a reduction in the pH of the ocean over an extended period,
typically decades or longer, which is caused primarily by uptake of car-
bon dioxide (CO2) from the atmosphere, but can also be caused by other
chemical additions or subtractions from ocean (Field et al., 2011). As
increased CO2 discharge, ocean acidification presented by decreased
⁎ Corresponding author.
E-mail address: changzige@ouc.edu.cn (C. Ge).
seawater pH value worsens (Yao et al., 2016). Seawater pH value reduc-
tion has been observed recently and widely (Ateweberhan et al., 2013;
Jin and Gao, 2016), and harmful algal blooms outbreak frequency in-
creases recently (Keesing et al., 2016; Weisberg et al., 2016). Moreover,
field experiments showed that the bottom water had high phosphate
concentration if the pH value was low (Cao et al., 2009). Thus, there
might be one correlation between ocean acidification and frequent out-
break of harmful algal blooms. Is ocean acidification one potential diver
for harmful algal blooms outbreak by increasing phosphate concentra-
tions of water body? The question is related to phosphorus cycle
under global climate change and measures to reduce ecological stress
caused by ocean acidification. However, there is few data about effects
of ocean acidification on increase of phosphate concentration in water
body especially in oxic conditions.
Thus, effects of ocean acidification on forms of phosphorous in oxic
sediments were measured in the present work to verify the hypothesis
that ocean acidification might lead to phosphorus eutrophication in
water body by changing forms of phosphorus in oxic sediments. The re-
sults may shed light on assessment of ocean acidification on phosphorus
cycle and control ecological stress caused by ocean acidification.
Moreover, the reasons resulting in harmful algal blooms should be
reconsidered.
2. Materials and methods
2.1. Sediment samples
Phosphorus is important for seagrasses which can resist ocean acid-
ification successfully (Fabricius et al., 2011; Koch et al., 2013) and it may
be one limited factor for seagrass in water area where phosphorus is

http://dx.doi.org/10.1016/j.marpolbul.2016.12.016
0025-326X/© 2016 Published by Elsevier Ltd.

Please cite this article as: Ge, C., et al., Ocean acidification: One potential driver of phosphorus eutrophication, Marine Pollution Bulletin (2016),
http://dx.doi.org/10.1016/j.marpolbul.2016.12.016
2 C. Ge et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

insufficient. One hypothesis that phosphorus released from sediments
promoted by ocean acidification might support the primary production
of seagrasses is established accordingly. Thus, sediments in seagrass
meadow were used in the present work. Zostera marina and surface sed-
iments with depth 20 cm were collected in one eelgrass meadow in
Shuangdao Bay (37°28′31″ N, 121°58′12″ E), Weihai, Shandong Prov-
ince, China. To ensure the sediments were oxic, these sampled sedi-
ments were mixed adequately and aerated for one day. Then, they
were put into plastic buckets with inside diameter 12 cm and height
22 cm. Moreover, the depth of sediment in these plastic buckets was
20 cm. Z. marina was cultured in these plastic buckets and the buried
root depth in sediments was 2 cm. Three plastic buckets were put into
one plastic box with size 60 × 40 × 35 cm. The coastal water sampled
from Shuangdao Bay with salinity 30‰ was put into the box. Moreover,
the distance between water and sediment surface was 10 cm. Water
flow with speed about 0.27 cm/s was drove by one water circulating
pump. Furthermore, the illumination intensity was 4500–5000
Lux andits period was 12 L:12 D. The water temperature with range
10–15 °C varied naturally. The aquatic system including sediments
and Z. marina was designed to acclimate the indoor conditions for one
month, however, it had to be kept for 5 months because of manpower
shortage and laboratory reconstruction. After five-month adaptation,
sediments in these buckets were poured out and the macro benthos
and stones were screened out. Then, these sediments were aerated
and mixed fully to determine effects of ocean acidification on forms of
phosphorus in oxic sediments.
2.2. Determination of the effects of ocean acidification on the forms of
phosphorus in the sediments
fluid was collected to determine the total phosphorus (TP) content in
sediments (mg/g) by the phosphomolybdate blue method (Li et al.,
2007).
The dried 0.10 g sediments were added into 25 mL HCl (0.10 mol/L).
After 2-h oscillation, the mixture was centrifuged at 4000 r/min
(3761 g) for 10 min and the supernatant was collected to determine
the phosphorous content in sediments (Pun-burned) (mg/g). Moreover,
the dried 0.10 g sediments were burned at 450 °C for 5.5 h. Then the
ashes were added into 25 mL HCl (0.10 mol/L). After 2-h oscillation,
the mixture was centrifuged at 4000 r/min (3761 g) for 10 min and
the supernatant was collected to determine the phosphorous content
in sediments (Pburned) (mg/g). The inorganic phosphorus (IP) content
in sediments (mg/g) was calculated by TP + Pun-burned − Pburned.
The dried 1.00 g sediments were added into 25 mL MgCl2
(1.00 mol/L). After 2-h oscillation, the mixture was centrifuged at
4000 r/min (3761 g) for 10 min. The supernatant fluid was sampled to
determine the exchangeable phosphorus (Ex-P) content in sediments
(μg/g) by the phosphomolybdate blue method (Zhang et al., 2013).
2.4. Statistical methods
To analyze effects of ocean acidification on forms of phosphorus in
sediments, One-way ANOVA was conducted if variances of contents of
phosphorus with different forms in sediments were homogeneous, dur-
ing which the multiple-comparison was conducted by the Bonferroni
test. Otherwise, the Dunnett-T3 test was used to compare effects of
ocean acidification on forms of phosphorus in sediments. The significant
level was 5%.

Uniform mixed sediments were put into plastic bucket with inside 3. Results
diameter 12 cm and depth 22 cm, which was put into one plastic box
with size 60 × 40 × 35 cm. Coastal water with salinity 30‰ sampled 3.1. TP and IP contents in sediments
from Shuangdao Bay was put into the box. The distance between
water and sediment surface was 15 cm. Moreover, the experimental After exposure to seawater with different pH for 30 days, the TP con-
water was filtered by degreasing cotton with water absorption ≥ 23. tent in sediments with depth 6 cm reduced as decreased seawater pH
Water flow with speed about 0.27 cm/s in the boxwas drove by one cir- value, however, the difference was not significant (Fig.1). The TP con-
culating pump. Moreover, the illumination intensity was 4500– tent in sediments exposed seawater with pH 8.1 was 1.52 ± 0.50
5000 Lux andits period was 12 L:12 D. The water temperature was (mean ± standard deviation) mg/g and that in sediments exposed to
about 20 °C and it varied naturally. According to the normal seawater ocean acidification with pH 7.7 was 1.29 ± 0.40 mg/g. IP content in
pH value and the ocean acidification trend (Riebesell et al., 2010), two sediments
pH values were set and they were 8.1 and 7.7, respectively.The normal The IP content in sediments with depth 6 cm significantly reduced as
water pH value is 8.1. Climate models predict additional declines of as decreased seawater pH values after the sediments was exposed to sea-
much as 0.3–0.4 pH units by the year 2100 (Doney et al., 2012), which water with different pH values for 30 days (p b 5%) (Fig.1). The IP con-
means that ocean acidification with pH 7.7 is projected to be observed tent in oxic sediments exposed to seawater with pH 8.1 was 1.39 ± 0.10
in the global ocean in 2100. Ocean acidification with pH 7.7 was simu- (mean ± standard deviation) mg/g, which was significantly higher than
lated by CO2 injection to seawater. The hyperpietic CO2 got into water that in sediments exposed to ocean acidification with pH 7.7 (1.06 ±
through high pressure tank (7 Mpa), pressure relief valve (YQT-3), sole- 0.20 mg/g) (p b 5%).
noid valve (TG22-08) and trim switch (SV-02). The CO2 aeration quan-
tity was controlled by pH control meter (Weipro pH-2010). Moreover,
there were three parallels for every treatment.
After exposure to seawater with different pH values 30 days, the sur-
face sediments with depth 6 cm were sampled by PVC pipe with inside
diameter 1.5 cm. During the 30 days, the pH 7.7 was maintained by con-
trolling CO2 aeration quantity. The seawater with pH 8.1 was left un-
treated and the measured pH was 8.11 ± 0.03 (mean ± standard
deviation).

2.3. Analysis of the forms of phosphorus in the sediments

Sediments exposed to seawater with different pHwere dried to con-

stant weight at 65 °C and the dried sediments were grinded slightly to
keep the natural grade size. The dried 0.10 g sediments were added
into 25 mL oxidant that consisted of K2S2O8 (0.15 mol/L) and NaOH
(0.15 mol/L). After 1-h nitration at 120 °C and 0.12 Mpa, the mixture
Fig. 1. TP and IP contents in sediments exposed to seawater with different pH values.
was centrifuged at 4000 r/min (3761 g) for 10 min. The supernatant

Please cite this article as: Ge, C., et al., Ocean acidification: One potential driver of phosphorus eutrophication, Marine Pollution Bulletin (2016),
http://dx.doi.org/10.1016/j.marpolbul.2016.12.016
 C. Ge et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx
Fig. 2. Ex-P content in sediments exposed to seawater with different pH values.
3.2. Ex-P content in sediments
The Ex-P content in sediments with depth 6 cm was 4.40 ± 0.45
(mean ± standard deviation) and 2.82 ± 0.15 μg/g, if the sediments
were exposed to seawater with pH 8.1 and ocean acidification with
pH 7.7, respectively (Fig.2). Thus, decreased seawater pH value reduced
Ex-P content in oxic sediments significantly (p b 5%).
4. Discussion
In one closed aquatic system, phosphorus is stored in two pools,
which is the water body and the sediments, respectively (Fig.3). The
phosphorus exchange between the two pools depends on phosphorus
diffusion flux across sediment-water interface, which is influenced by
seawater pH and the forms of phosphorus in sediments (Freitas et al.,
2014; Lai, 2014). Before the aquatic system is exposed to ocean acidifi-
cation, the IP and OP content in water body and sediments is WIP, WOP,
SIP and SOP, respectively. After ocean acidification, the IP and OP content
in water and sediments is WAIP, WAOP, SAIP and SAOP, respectively. As the
phosphorus biogeochemical cycle belongs to sedimentary cycle, one
material balance equation is obtained, WIP + WOP + SIP + SOP =
WAIP + WAOP + SAIP + SAOP, which means that SIP − SAIP =
WAIP + WAOP − WIP − WOP + SAOP − SOP. IF the OP content in sediment
is relative low and the mineralization of OP can be neglected, the re-
duced phosphorus accumulated in sediments may diffuse into water
body or it may be used by aquatic organisms in water body.
Through its role as a major factor controlling sediment pH value,
ocean acidification can regulate the biogeochemical behavior of phos-
phorus in sediments (Tsukasaki et al., 2015). Phosphorus accumulated
in sediments includes organic phosphorus and inorganic phosphorus.
Although phytoplankton and bacteria can use organic phosphorus di-
rectly (Spohn et al., 2015; Zhou et al., 2016), inorganic phosphorus is
Fig. 3. Phosphorus pools and forms of phosphorus in sediments.
Please cite this article as: Ge, C., et al., Ocean acidification: One potential driver of phosphorus eutrophication, Marine Pollution Bulletin (2016),
http://dx.doi.org/10.1016/j.marpolbul.2016.12.016
3
the dominant forms of phosphorus that can be used by aquatic botany
directly and almost all organic phosphorus can be used by aquatic bot-
any only after mineralization. Alkaline conditions can accelerate organic
phosphorus mineralization which slowed down when environment is
neutral (Li et al., 2011). If water pH value ranges from 5.5 to 8.5, organic
phosphorus mineralization rate decreases as decreased water pH value
and the organic phosphorus mineralization rate can be expressed by
y = 2.15x + 81.60 (R2 = 99.84 × 10−2, p b 5%), where xand yis water
pH value and mineralization rate (%), respectively (Song et al., 2011a).
In the present work, the set seawater pH was 7.7 and 8.1, which
meant that the mineralization rate of organic phosphorus decreased
0.86% if the pH value decreased from 8.1 to 7.7. In the present work,
the ratio of IP/TP in sediments exposed to seawater with pH value 8.1
was 91.45%. Thus, the effect of ocean acidification on organic phospho-
rus mineralization might be ignored in the present work.
The TP content in sediments in Ardmucknish Bay, Scotland, in spring
and summer of 2012 was not sensitive to CO2 concentration (Tsukasaki
et al., 2015), which means that responses of phosphorus forms to ocean
acidification depends on phosphorus forms. The inorganic phosphorus
in sediments includes weakly adsorbed phosphorus (W-P), aluminum
and iron bound phosphorus (Al-P and Fe-P), authigenic calcium phos-
phorus (Ca-P) and occluded phosphorus (O-P) (Xu et al., 2011). O-P is
inert and it is not influenced by H+ concentration variation, which im-
plies that O-P will not vary with pH value. Ca-P is the kind of phosphorus
that is united with calcium carbonate, which may dissolve as H+ con-
centration increases (Cyronak and Eyre, 2016). Al-P and Fe-P are the
phosphorus that combined with Al(OH)3 or Fe(OH)3, which may dis-
solve in acidic conditions. Thus, if the H+ concentration increases, Ca-
P, Al-P and Fe-P may transform into W-P, which may be exchanged by
positive ions considered as exchangeable phosphorus (Wang et al.,
2015). As carbon dioxide dissolves in seawater, it reacts with water in
accordance with following chemical equilibria, CO2 (g) = CO⁎2 (aq),
CO⁎2 (aq) + H2O = H+(aq) + HCO− −
3 (aq), and HCO3 (aq) = H
+
2–
(aq) + CO3 (aq), where g and aq refer the state of the species. Under
ocean acidification, positive ions such as H+ concentrations increase
and Ex-P diffuses across sediment-water interface into water body.
Thus, there were relative low content of Ex-P or IP in sediments exposed
to seawater with pH 7.7 in the present work. Moreover, the decreased
pH value promotes phosphorus diffusion flux across sediment-water in-
terface (Chen et al., 2014) and the phosphorus concentration of water
column is negative related to pH values significantly (Zhu and Fang,
2014), which implies the phosphorus diffusion from sediment to
water body may be related to ocean acidification in some extent.
Sediment is an important phosphorus sink in the oceanic phospho-
rus cycle (Filippelli, 2001), and sediment plays an essential role in regu-
lating phosphorus availability in shallow coastal zones through
phosphorus release to and uptake from the water column, which play
an important role for alga bloom. According to field investigations, pri-
mary production is limited by phosphorus in many water areas
(Powley et al., 2014; Li et al., 2015). The species of marine organisms
4 C. Ge et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx
that lead to harmful algal blooms belong to opportunistic species and
they may mass multiply if the phosphorus concentration increases in
the phosphorus limitation areas (Yamaguchi et al., 2008). Just as results
of Tsukasaki et al. (2015), during which the ocean acidification was in-
duced by injection CO2 into sediments, the TP content in sediments
was not significantly influenced by ocean acidification in the present
work. Nevertheless, the contents IP and Ex-P which has highest bioac-
tivity in oxic sediments decreased significantly as sediments were ex-
posed to ocean acidification with pH 7.7. According to material
balance, these reduced phosphorus in sediments diffused into water
body or were used by aquatic organisms, which meant that active phos-
phorus released from the oxic sediment phosphorus pool into the water
body pool. IF the OP content in sediments is relative low and the miner-
alization of OP can be neglected, the released DIP from sediments might
be estimated by 1 − SAIP / SIP. According to results of the present work,
the released DIP accounted 23.74% of IP in sediments and it was estimat-
ed by 1 − IP7.7 / IP8.1, where IP7.7 and IP8.1 was the IP content in sedi-
ments exposed to seawater with pH 7.7 and 8.1, respectively. Thus,
effects of ocean acidification on phosphorus concentration increase
might be calculated by IP × SW × 23.74 / (100 × V), where SW and V
was sediment weight and water body volume. As phosphorus limitation
in ocean are widespread (Baek et al., 2015; Zhang et al., 2015), ecologi-
cal effects of phosphorus diffusion flux across oxic sediment on algal
bloom can't be ignored and ocean acidification is one potential driver
for phosphorus eutrophication in oxic conditions.
Acknowledgements
The authors are grateful for financial support from the Science & Tech-
nology Project of Shandong Province (2014GSF117042), China Postdoc-
toral Science Foundation (2013M541905) and the Science & Technology
Project of Shenzhen under contract (JCYJ2014041811549187).
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.marpolbul.2016.12.016.
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Please cite this article as: Ge, C., et al., Ocean acidification: One potential driver of phosphorus eutrophication, Marine Pollution Bulletin (2016),
http://dx.doi.org/10.1016/j.marpolbul.2016.12.016