Marine Pollution Bulletin xxx (2014) xxx–xxx

Contents lists available at ScienceDirect

Marine Pollution Bulletin journal homepage:


The positive relationship between ocean acidification and pollution Xiangfeng Zeng a,b, Xijuan Chen a, Jie Zhuang a,c,⇑ a

Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China University of Chinese Academy of Sciences, Beijing 100039, China c Department of Biosystems Engineering and Soil Science, The University of Tennessee, Knoxville, TN 37996, USA b

a r t i c l e

i n f o

Article history: Available online xxxx Keywords: Ocean acidification Pollution Heavy metal Oil Biotoxicity Carbon dioxide

a b s t r a c t Ocean acidification and pollution coexist to exert combined effects on the functions and services of marine ecosystems. Ocean acidification can increase the biotoxicity of heavy metals by altering their speciation and bioavailability. Marine pollutants, such as heavy metals and oils, could decrease the photosynthesis rate and increase the respiration rate of marine organisms as a result of biotoxicity and eutrophication, facilitating ocean acidification to varying degrees. Here we review the complex interactions between ocean acidification and pollution in the context of linkage of multiple stressors to marine ecosystems. The synthesized information shows that pollution-affected respiration acidifies coastal oceans more than the uptake of anthropogenic carbon dioxide. Coastal regions are more vulnerable to the negative impact of ocean acidification due to large influxes of pollutants from terrestrial ecosystems. Ocean acidification and pollution facilitate each other, and thus coastal environmental protection from pollution has a large potential for mitigating acidification risk. Ó 2014 Elsevier Ltd. All rights reserved.

Contents 1. 2.



Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pollution-facilitated ocean acidification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Pollutants decrease anthropogenic CO2 uptake by marine organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Eutrophication enhances acidification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acidification enhances marine pollution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Acidification increases the biotoxicity of heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Acidification reduces degradation of organic pollutants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Closing remarks and future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Increasing atmospheric CO2 concentrations cause a net air-to-sea flux of excess CO2, leading to predictable changes in the biogeochemical cycles of many elements and the chemistry of seawater. Changes include increases in the partial pressure of

⇑ Corresponding author at: Department of Biosystems Engineering and Soil Science, The University of Tennessee, Knoxville, TN 37996, USA. Tel.: +1 (865) 974 1325. E-mail address: [email protected] (J. Zhuang).

00 00 00 00 00 00 00 00 00 00

CO2 (pCO2), decreases in pH, and decreases in the carbonate h i concentration CO23 . This net flux process, known as ocean acidification, is often referred to as ‘‘the other CO2 problem’’ (Doney et al., 2009). Relative to preindustrial levels, contemporary surface ocean pH has dropped, on average, by about 0.1 pH units (a 26% increase in [H+]). A further decline of 0.2–0.3 pH units will occur over the 21st century unless human CO2 emissions are curtailed substantially (Orr et al., 2005). Ocean acidification could significantly influence marine ecosystems (Gattuso and Hansson, 2011). One well-known effect is the lowering of the calcium carbonate saturation state, which impacts shell-forming marine organisms, 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Zeng, X., et al. The positive relationship between ocean acidification and pollution. Mar. Pollut. Bull. (2014), http://


X. Zeng et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

from plankton to benthic mollusks, echinoderms, and coral (Hughes et al., 2003; Hoegh-Guldberg et al., 2007; Pandolfi et al., 2011). Ocean acidification alters phytoplankton abundance and carbon fixation rates in some photosynthetic organisms (both calcifying and non-calcifying) (Doney et al., 2009). For instance, many calcifying species exhibit reduced calcification and growth rates in laboratory experiments under high-CO2 conditions (Feely et al., 2010). Since photosynthesis is the major consuming process of carbon dioxide, any change in phytoplankton abundance could exert a feedback effect on the overall carbon dioxide balance between the atmosphere and the ocean (Nikinmaa, 2013). Acidification-induced changes in the attributes of marine ecosystems do not occur in isolation. Non-CO2 anthropogenic inputs (e.g., pollution) also contribute significantly to the overall acidification threat in some coastal regions (Feely et al., 2010; Cai et al., 2011). Human fossil fuel combustion, fertilizer use, and industrial activity cause a continuous influx of pollutants (e.g., heavy metals, oil hydrocarbons, persistent organic pollutants, pesticides, and eutrophication nutrient elements) into marine ecosystems (Fig. 1). Heavy metals, such as mercury (Hg) and lead (Pb), are the most common types of coastal contaminants detected in relatively high concentrations in waters and sediments of many coastal and estuarine systems (Doney et al., 2009). They can bioaccumulate in the fatty tissues of marine organisms and pass up the food chain to threaten human health through the consumption of contaminated food products, including predatory fish, marine mammals, and seabirds (Elliott and Elliott, 2013; Mostofa et al., 2013). As for oil hydrocarbons, natural seepage alone introduces about 6  105 metric tons of crude oil to oceans every year, representing 47% of all crude oil entering the marine environment. The remaining 53% of crude oil contamination results from anthropogenic activities (e.g., accidental oil spills and transport activities) (Kvenvolden and Cooper, 2003). Exploration of geological phosphate reserves for fertilizer production creates a largely one-way flow of phosphorus from rocks to farms and then to oceans, dramatically increasing eutrophication (Fig. 1). Globally, oxygendepleted marine coastal ‘‘dead zones’’ caused by eutrophication continue to expand (Diaz and Rosenberg, 2008; Bennett and Elser, 2011). The Gulf of Mexico’s ‘‘dead zone,’’ averaging more than 17,000 square kilometers in recent years, is forecast to continuously increase (Bennett and Elser, 2011; Slomp, 2011). Considering the coexistence of ocean acidification and pollution in many coastal regions, these two processes may have combined effects on marine ecosystems in the foreseeable future. Changes in the speciation of heavy metals with water pH could affect the

Fig. 1. Interactions between ocean acidification (red) and pollution (blue). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

bioavailability and toxicity of those metals (Diaz and Rosenberg, 2008; Millero, 2009). Meanwhile, heavy metals could also influence the rates of photosynthesis and respiration, causing changes in the levels of carbon dioxide and oxygen in seawater. Therefore, when evaluating the impacts of ocean acidification on marine ecosystems, changes in the bioavailability and toxicity of pollutants with changes in pH and oxygenation must be considered. This review aims to summarize relevant information for an insightful analysis of the interactions between ocean acidification and pollution in relation to other stressors to marine ecosystems.

2. Pollution-facilitated ocean acidification 2.1. Pollutants decrease anthropogenic CO2 uptake by marine organisms The effect of pollutants on the abundance of photosynthetic organisms (in comparison to heterotrophs) and their photosynthesis could eventually change the role of ocean autotrophs in global carbon dioxide dynamics as carbon dioxide sinks (Macdonald et al., 2005; Nikinmaa, 2013). Pollutants generally decrease the rate of photosynthesis and in turn CO2 uptake by ocean phytoplankton (Fig. 1). As an indirect result, the amount of atmospheric CO2 increases and becomes available for absorption by seawater to enhance acidification. The presence of heavy metals in oceans may inhibit primary production in marine ecosystems and decrease the efficiency of carbon dioxide removal from the atmosphere. Most previous studies have been performed in laboratory cultures (see Table 1). For instance, after 48 h of exposure to 0.031 mg/L of Cu2+ for Microcystis aeruginosa (M. aeruginosa) and 0.047 mg/L of Cu(II) for Chlorella vulgaris (C. vulgaris), the percentage of cell autofluorescencing decreased, while 0.064 mg/L of Cu(II) decreased both photosynthesis rates and growth rates by 50% (Hadjoudja et al., 2009). Exposure to 50 mg/L and 80 mg/L of Pb(II) for 120 h significantly inhibited the contents of Chlorophyll a (chl a) in Chlorella protothecoides (C. protothecoides) by 65% and 49%, respectively (Xiong et al., 2013). When the concentrations of Cd(II) exceed 2.02  10 4 mg/L and 3.60  10 4 mg/L, the growth of Thalassiosira pseudonana (T. pseudonana), Prorocentrum minimum (P. minimum), and Chlorella autotrophica (C. autotrophica) was significantly slower (Wang and Wang, 2009). At 0.03 mg/L of Hg(II), the growth rate of C. autotrophica, Isochrysis galbana (I. galbana), and Thalassiosira weissflogii (T. weissflogii) decreased significantly (p < 0.05), with calculated LC50 values 0.05 mg/L, 0.09 mg/L, and >0.10 mg/L, respectively (Wu and Wang, 2011; Wu and Wang, 2014). These studies are partially comparable because of the use of a few of the same species and standards in laboratory setups. However, due to the higher concentrations used in the experiments than would be found in natural seawater, bioavailability and biotoxicity of the above heavy metals might be underestimated relative to natural scenarios. Debelius et al. (2011) exposed Synechococcus Populations, which were collected from different geographic sites and depths in the Strait of Gibraltar, to solutions of Cu, Ni, and Zn and found that the EC50 value of Cu was as low as (4.4 ± 0.4)  10 3 mg/L for surface Atlantic water populations and as low as (5.9 ± 0.9)  10 4 mg/L for surface Mediterranean water populations. The LC50s varied from 0.23 mg/L (Atlantic Prochlorococcus) to 498.7 mg/L (Black Sea picoeukaryotes) for Cd and from 20.02 mg/L (Mediterranean Synechococcus) to 465.2 mg/L (Black Sea nanoplankton) for Pb (Echeveste et al., 2012). For chl a, the LC50 of Cd varied from 0.81 mg/L in the Atlantic Ocean to 560 mg/L in the Black Sea, while the LC50s of Pb were much greater, 3080 mg/L and 9240 mg/L, for the Black Sea and Atlantic Ocean experiments, respectively. These results indicate a higher toxicity of Cd than Pb to phytoplankton grown in those seawaters

Please cite this article in press as: Zeng, X., et al. The positive relationship between ocean acidification and pollution. Mar. Pollut. Bull. (2014), http://


X. Zeng et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx Table 1 Experimental evidence on the interactions between ocean acidification and pollution. Pollutant


Pollution-facilitated ocean acidification Cu M. aeruginosa and C. vulgaris Natural phytoplankton Pb C. protothecoides and C. vulgaris Natural phytoplankton Cd T. pseudonana, P. minimum and C. autotrophica Natural phytoplankton Hg C. autotrophica, I. galbana, and T. weissflogii Ni Natural phytoplankton Zn Natural phytoplankton Oil Marine phytoplankton

Dosing protocol



0.0195–0.635 mg/L


Hadjoudja et al. (2009) Debelius et al. (2011) Xiong et al. (2013) Echeveste et al. (2012, 2014) Wang and Wang (2009)

0, 2, 8, 15 and 30  10



1, 5, 10, 50, and 80 mg/L


Dose–response relationships were clearly observed

0.01, 0.02, 0.1, 1.12, 11.2, 112, and 1000  10 3 mg/L 1.12  10 3 to 6.63 mg/L


Cell abundances and growth rates decreased


The growth was significantly restrained.

0.01, 0.02, 0.1, 1.12, 11.2, 112, and 1000  10 3 mg/L 7.86  10 3 to 0.1114 mg/L


Cell abundances and growth rates decreased


Growth rate decreased significantly at 0.03 mg/L



Different toxic effects belonging to different sampling locations.



Different toxic effects belonging to different sampling locations

0, 20, 100, 250 and 600  10 mg/L 0, 20, 100, 250 and 600  10 mg/L 0.18–9.94 mg/L 0, 0.010, 0.05, 0.1 ml/L


Marine phytoplankton


T. pseudonana


0–250 mg/L

0.0025–0.5 mg/L for Pyr, 0.003– 3 mg/L for Flu, and 5  10 5– 0.328 mg/L for BaP. Water samples collected in August 7, 2010, following the accidental oil spill in Mumbai Harbour


Water samples collected in February and August 2008


Data collected in northern Gulf of Mexico and East China Sea and assessed with biogeochemical model. Water samples collected in Gulf of Mexico and the Baltic Sea. Data analyzed with AOU calculation-based biogeochemical model. Data collected in the estuaries of Amazon, Mississippi, and St. Johns. The MatLabÒ version of the program CO2SYS was used to run the simulations.



Acidification-enhanced marine pollution Cu A. atopus


Hard shell clams (M. mercenaria) C. virginica and M. mercenaria Cuttlefish eggs C. virginica and M. mercenaria M. mercenaria

Zn Ag Co

Cuttlefish eggs

Hg Mn Fe, Co, Cu, Zn, Pb, Cd, Ni, Cr Pb, Cd, Cu and Zn Fe(III)

P. tricornutum

Cell division rate and autofluorescence decreased as copper concentrations increased Different toxic effects were observed different sampling locations


Echeveste et al. (2012, 2014) Wu and Wang (2011, 2014)


The growth was restrained, when concentrations of crude oil was over 4.68 mg/L Total phytoplankton biomass declined, altered phytoplankton community i CorexitÒ EC9500A alone had a highly inhibitory effect, and increased the amount of oil in water i Dose–response curves for growth inhibition were determined. i

d Concentration of chlorophyll a decreased from 2.4–39.2 to 0.8– 1.5 mg/m3, and the ratios of chlorophyll a to phaeophytin decreased from 2.7–8.0 to 0.8–0.9 d The pH value in surface and subsurface waters were 7.71–7.75 and 99% of Fe and Cu, >98% of Zn, and >70% of Cd are bound to organic molecules (Rue and Bruland, 1995; Saito et al., 2005; Baars and Croot, 2011). The effect of pH on the speciation of metal–organic complexes in the marine environment is not as well characterized as the inorganic ligands due to their heterogeneous composition and the unknown structure of the organic ligands. Two classes of organic ligands, classified as L1 (type-I) and L2 (type-II) ligands, coexist in seawater. Louis et al. (2009) assessed the effect of pH on the stability constants in the formation of organic complexes. They reported a lower Cu(II)–organic complex constant (log KCuL = 9.9) and found that the concentration of the L1 ligand decreased by 25% between pH 8.1 and 7.4. Based on this decrease, Millero (2009) estimated the effect of pH on the speciation of Cu(II) in seawater and found that the levels of free copper may surpass the 6.4  10 8 mg/L threshold, a level toxic to some organisms. Change in pH also affects the rates of oxidation and reduction of metals (e.g., Cu and Fe) and photochemical processes (e.g., production of HO2, O2 , and H2O2). Acidification usually increases reduction rates more than oxidation rates, as the latter is less pH dependent. For example, the half-life of Fe(II) in seawater increases from one minute to 24 min when pH decreases from 8.1 to 7.4 (Millero, 2009). These results imply that ocean acidification could increase the amount of reduced metals (e.g., Cu(I) and As (III)), which are much more toxic to the biota than their oxidized states (De Orte et al., 2014b). Cu, Cd, and Pb are toxic at certain concentrations in the marine environment. Their ambient concentrations in the open ocean are low, but a small increase often leads to toxic effects on the organisms that are unaccustomed to the change (Morel et al., 2006). This has been observed with the free form of Cu(II) at concentrations as low as 6.4  10 8 mg/L, which were reported to be toxic to marine phytoplankton (Brand et al., 1986). So far it is not known whether ocean acidification could affect Cu ligand production and its biotoxicity. Modeling research predicted that the mean Cu(II) concentration in the estuary could increase by 115% over the next 100 years as a result of the projected decrease in ocean pH (Richards et al., 2011). The results suggest that Cu toxicity for phytoplankton growth occurs at decreasing pH. Pascal et al. (2010)


observed an increased toxicity of Cu to the copepod Amphiascoides atopus (A. atopus) under conditions of elevated pCO2. Recent studies have also shown that ocean acidification can affect toxicity, accumulation, and intracellular binding of metals in marine organisms (Lacoue-Labarthe et al., 2009; Pascal et al., 2010; Campbell et al., 2014). Lacoue-Labarthe et al. (2009, 2011, 2012) reported that ocean acidification could affect the bioaccumulation of heavy metals, radionuclides, and trace elements in the eggs and embryos of the squid L. vulgaris and in the eggs of the cuttlefish Sepia officinalis. Their results demonstrated a pH effect on the adsorption and protective properties of the eggshell and an elevated pCO2 effect on the metabolism of embryo and paralarvae, both leading to metal accumulation in the tissues of Loligo vulgaris (L. vulgaris). Ivanina and Sokolova (2013) found that elevated pCO2 significantly but differently affected the accumulation of Cu and Cd in isolated mantle cells of hard clams Mercenaria mercenaria (M. mercenaria L). Acidification can also change the physiological consequences of metals for organisms in a species–specific manner, eventually influencing their fitness and survival. Götze et al. (2014) reported that elevated pCO2 enhanced accumulation of Cu and Cd in the gills of mollusk and that the simultaneous exposure to Cu and pCO2 (800 latm) led to an increase in AMP and a decline in the levels of glycogen, ATP, and ADP. The AMP enhancement indicates an increase in energy deficiency as a result of the combined exposure to Cu and elevated pCO2. Ivanina et al. (2014) found that elevated pCO2 along with Cd exposure resulted in decreases in phagocytic activity, adhesion capacity, and expression of mRNA for lectin and heat shock protein (HSP70) in clam and oyster hemocytes. These studies suggest that elevated pCO2 potentiates the negative effects of heavy metals on immunity and may further sensitize organisms to other stresses, such as pathogens and diseases, during ocean acidification in polluted estuaries. Currently, little is known about the potential impact of ocean acidification on the behavior of metals bound to sediments, where metals accumulate to greater concentrations than in the overlying water. Acidification can indirectly alter the conditions and properties of bottom sediments, causing changes in the geochemical fluxes of major and trace elements at the sediment-seawater interface. Decreasing pH and Eh close to CO2 vents may affect the solubility, bioavailability, and toxicity of redox-sensitive elements, exerting harmful effects on marine ecosystems (Kadar et al., 2012; Basallote et al., 2014). Ardelan and Steinnes (2010) and Ardelan et al. (2012) examined the role of elevated CO2 in controlling fluxes of labile metals from contaminated sediments. They found that ‘‘dissolved’’ concentrations of seven metals (Al, Cr, Ni, Pb, Cd, Cu, and Zn) increased substantially in water during the first phase (16 days). The results of De Orte et al. (2014a) showed that sediment acidification enhanced the release of metals to elutriates, with diatom growth inhibited by both acidification and the presence of metals. Toxicity tests involving sediment-bound Cu demonstrated enhanced Cu mobilization at pH 4 relative to pH 7. As pH decreases, Cu bioavailability increases due to increases in its free form. Roberts et al. (2013) reported that labile Ni and Zn increased in the pore water of sediment, with amphipod DNA damage 2.7 times higher in an increased pCO2 (750 latm) scenario. However, the toxicological interaction between ocean acidification and contaminants could not be completely interpreted by the effects of pH on metal speciation. Additive physiological effects of ocean acidification and contaminants might be more important than the change in metal speciation for determining the responses of benthos to contaminated sediments under ocean acidification. The majority of the above mentioned studies were performed in laboratories, assuming that ocean acidification is a very slow process. In order to understand the in-situ effects of ocean acidification on metal bioavailability, volcanic vents in shallow submarine were used in a number of investigations as models or analogues

Please cite this article in press as: Zeng, X., et al. The positive relationship between ocean acidification and pollution. Mar. Pollut. Bull. (2014), http://


X. Zeng et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Fig. 3. Interactive mechanisms of acidification with metals, oil, organic matter, and organisms.

for studying the prospective impacts caused by pH and pH-beyond mechanisms (Vizzini et al., 2013; Kerfahi et al., 2014; Milazzo et al., 2014). For instance, Vizzini et al. (2013) determined the levels of trace elements in seafloor sediments and in the tissues of a local seagrass (Cymodocea nodosa) and its epiphytes across a spatial pH gradient in the vicinity of a volcanic seep in Levante Bay on Vulcano Island in northeast Sicily, Italy. Their results indicated that concentrations of As, Ba, Hg, Mo, Ni, Pb, and Zn were generally greatest in the locations close to the primary CO2 vent. They also observed localized bioenrichment of three trace elements (Cd, Hg, and Zn) in both epiphytes and epiphyte-harboring seagrass. McClintock et al. (2014) reported similar results on the accumulation of trace elements (As, Cd, Co, Cr, Hg, Mo, Ni, Pb and V) in shells (an established proxy for tissues) of four species of gastropods (two limpets, a top shell, and a whelk), which were collected from three sites in Levante Bay, Vulcano Island, Italy. 3.2. Acidification reduces degradation of organic pollutants Ocean acidification affects organic degradation due to an alteration of metal speciation and nutrient bioavailability (Fig. 3). Since few studies have addressed these influences, we assessed them based on indirect evidence. Iron is an important contributing factor to the detoxification of hydrocarbons. It could affect the enzyme activity necessary to catalyze oxidative breakdowns of organic pollutants (e.g. PAHs) and oils (Santos et al., 2008). Monooxygenase and dioxygenase enzymes, essential for most microbial pathways of PAHs and oil degradation, require a metal cofactor, which is often iron (Bugg, 2003). The activity of a few key enzymes, such as toluene monooxygenase, in the degradation of the aromatic hydrocarbon toluene by Pseudomonas putida, was found to reduce under iron-limiting conditions (Dinkla et al., 2001; Bugg, 2003). The Deep water Horizon oil spill resulted in a massive influx of hydrocarbons into the Gulf of Mexico, and the addition of FeCl2 initially increased respiration rates and oil degradation (Bælum et al., 2012). However, Shi et al. (2010) reported that the predicted pCO2 level for the year 2100 would reduce biologically available Fe(III) by 10–20%, due likely to pH-induced binding of iron to organic ligands. The reduction in iron bioavailability due to ocean acidification would thus have potentially harmful effects on the degradation of organic pollutants and oils. Nitrogen is a key factor that facilitates detoxification of PAHs and degradation of other organic pollutions (Shi et al., 2012). As one of the most important sources of nitrogen in open ocean, fixed nitrogen is a nutrient that limits the growth of photosynthetic organisms (primary producers), such as algae and marine bacteria, and serves as an energy source or an

oxidant for marine bacteria and archaea (Xu et al., 2012). Ocean acidification decreased the efficiency of nitrogen fixation in the model marine cyanobacterium Trichodesmium, a dominant N2 fixer in the oceans (Shi et al., 2012; Xu et al., 2012). Moreover, nitrification rates can decrease to zero at pH 6.0–6.5, as the NH3 substrate disappears from the system (Huesemann et al., 2002; Mostofa et al., 2013). Elevated atmospheric CO2 has been reported to cause a decline in ocean oxygen levels (Diaz and Rosenberg, 2008; Hofmann and Schellnhuber, 2009; Rabalais et al., 2014). Oxygen is one of the most essential elements in microbial degradation of hydrocarbons and necessary for the initial breakdown of hydrocarbons. The lower oxygen level reduces microbial activities, resulting in lower degradation and even causing anaerobic degradation, which has a lower degradation rate under ordinary circumstances (Erses et al., 2008). On the other hand, organic pollutants in the ocean can be adsorbed or bound by colloidal organic matter and fixed in an organic–metal–mineral complex. Over 50% of organic matter was bound in organic–metal–mineral complexes in the ocean (Jurado et al., 2005). The dissolution of metal ions due to ocean acidification could destroy organic–metal complexes and accordingly promote the release and toxicity of organic pollutants. The increased bioavailability and toxicity of heavy metals due to acidification could hinder the biodegradation of organic contaminants (Sandrin and Maier, 2003; Erses et al., 2008). The presence of heavy metals inhibited 1,2-dichloroethane biodegradation in a dose-dependent manner, with the following order of decreasing inhibitory effect: Hg2+ > As3+ > Cd2+ > Pb2+ (Olaniran et al., 2011). Addition of Cu to estuarine sediments could decrease the abundance of hydrocarbon degrading microorganisms and the corresponding degradation rates. For instance, no degradation was observed at a Cu level of 270 mg/Kg (dry sediment) (Almeida et al., 2013). 4. Closing remarks and future directions The limited experimental data gathered so far suggests that there might exist a positive correlation between ocean acidification and pollution. Ocean acidification has considerable potentials for increasing the bioavailability and biotoxicity of heavy metals and reducing the degradation of organic pollutants by altering metal speciation and nutrient bioavailability. On the other hand, heavy metals and oils decrease the rate of photosynthesis, whereas eutrophication increases respiration, both leading to ocean acidification. Overall, marine pollution increases the susceptibility of coastal waters to ocean acidification. Currently, the interactions between ocean acidification and pollution have not been well addressed because of scarce relevant information. Further study is required to identify the interactive mechanisms of metals and organics with ocean acidification at multiple spatiotemporary scales. For this, the data collected from estuarine, coast, and open ocean are especially useful. Although the dominant biogeochemical processes in the ocean do not fundamentally alter under higher CO2/lower pH conditions, the microbial adaptability to other environmental stresses, like pollution, is weakened as ocean acidifies. Therefore, it is essential to systematically explore the synergistic effects between ocean acidification and pollutants on biological response and acclimation, especially in the coastal zones. With ocean acidification and pollution and their interactions becoming major concerns, coastal pollution control is a potential tool for mitigating the risk of ocean acidification. Acknowledgments This work was financially supported by the strategic priority research program of the Chinese Academy of Sciences (Grant No.

Please cite this article in press as: Zeng, X., et al. The positive relationship between ocean acidification and pollution. Mar. Pollut. Bull. (2014), http://

X. Zeng et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

XDB14020204) and a visiting scholarship of China Scholarship Council. The authors thank Zhiwang Yuan and Zhe Xu for their help with figure drawing and information collection. References Aksmann, A., Tukaj, Z., 2008. Intact anthracene inhibits photosynthesis in algal cells: A fluorescence induction study on Chlamydomonas reinhardtii cw92 strain. Chemosphere 74, 26–32. Almeida, R., Mucha, A.P., Teixeira, C., Bordalo, A.A., Almeida, C.M.R., 2013. Biodegradation of petroleum hydrocarbons in estuarine sediments: metal influence. Biodegradation 24, 111–123. Ardelan, M., Steinnes, E., 2010. Changes in mobility and solubility of the redox sensitive metals Fe, Mn and Co at the seawater–sediment interface following CO2 seepage. Biogeosciences 7, 569–583. Ardelan, M.V., Sundeng, K., Slinde, G.A., Gjøsund, N.S., Nordtug, T., Olsen, A.J., Steinnes, E., Torp, T.A., 2012. Impacts of possible CO2 seepage from sub-seabed storage on trace elements mobility and bacterial distribution at sediment– water interface. Energy Proc. 23, 449–461. Baars, O., Croot, P.L., 2011. The speciation of dissolved zinc in the Atlantic sector of the Southern Ocean. Deep-Sea Res. II. 58, 2720–2732. Basallote, M.D., De Orte, M.R., DelValls, T.Á., Riba, I., 2014. Studying the effect of CO2-induced acidification on sediment toxicity using acute amphipod toxicity test. Environ. Sci. Technol. 48, 8864–8872. Bejarano, A.C., Levine, E., Mearns, A.J., 2013. Effectiveness and potential ecological effects of offshore surface dispersant use during the Deepwater Horizon oil spill: a retrospective analysis of monitoring data. Environ. Monit. Assess. 185, 10281–10295. Bælum, J., Borglin, S., Chakraborty, R., Fortney, J.L., Lamendella, R., Mason, O.U., Auer, M., Zemla, M., Bill, M., Conrad, M.E., 2012. Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ. Microbiol. 14, 2405– 2416. Bennett, E., Elser, J., 2011. A broken biogeochemical cycle. Nature 478, 29–31. Bopp, S.K., Lettieri, T., 2007. Gene regulation in the marine diatom Thalassiosira pseudonana upon exposure to polycyclic aromatic hydrocarbons (PAHs). Gene 396, 293–302. Brand, L.E., Sunda, W.G., Guillard, R.R., 1986. Reduction of marine phytoplankton reproduction rates by copper and cadmium. J. Exp. Mar. Biol. Ecol. 96, 225–250. Bugg, T.D., 2003. Dioxygenase enzymes: catalytic mechanisms and chemical models. Tetrahedron 59, 7075–7101. Cai, W.J., Hu, X., Huang, W.J., Murrell, M.C., Lehrter, J.C., Lohrenz, S.E., Chou, W.C., Zhai, W., Hollibaugh, J.T., Wang, Y., 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766–770. Caldeira, K., Wickett, M.E., 2003. Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365–365. Campbell, A.L., Mangan, S., Ellis, R.P., Lewis, C., 2014. Ocean acidification increases copper toxicity to the early life history stages of the polychaete arenicola marina in artificial seawater. Environ. Sci. Technol. 48, 9745–9753. De Orte, M.R., Lombardi, A.T., Sarmiento, A.M., Basallote, M.D., Rodriguez-Romero, A., Riba, I., Del Valls, A., 2014a. Metal mobility and toxicity to microalgae associated with acidification of sediments: CO2 and acid comparison. Mar. Environ. Res. 96, 136–144. De Orte, M.R., Sarmiento, A.M., Basallote, M.D., Rodríguez-Romero, A., Riba, I., delValls, A., 2014b. Effects on the mobility of metals from acidification caused by possible CO2 leakage from sub-seabed geological formations. Sci. Total Environ. 470, 356–363. Debelius, B., Forja, J., Lubián, L., 2011. Toxicity of copper, nickel and zinc to Synechococcus populations from the Strait of Gibraltar. J. Mar. Syst. 88, 113–119. Diaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929. Dinkla, I.J., Gabor, E.M., Janssen, D.B., 2001. Effects of iron limitation on the degradation of toluene by Pseudomonas strains carrying the TOL (pWWO) plasmid. Appl. Environ. Microbiol. 67, 3406–3412. Doney, S.C., Fabry, V.J., Feely, R.A., Kleypas, J.A., 2009. Ocean acidification: the other CO2 problem. Mar. Sci. 1, 169–192. Echeveste, P., Agustí, S., Tovar-Sánchez, A., 2012. Toxic thresholds of cadmium and lead to oceanic phytoplankton: cell size and ocean basin–dependent effects. Environ. Toxicol. Chem. 31, 1887–1894. Echeveste, P., Tovar-Sánchez, A., Agustí, S., 2014. Tolerance of polar phytoplankton communities to metals. Environ. Pollut. 185, 188–195. Elliott, J.E., Elliott, K.H., 2013. Tracking marine pollution. Science 340, 556–558. Erses, A.S., Onay, T.T., Yenigun, O., 2008. Comparison of aerobic and anaerobic degradation of municipal solid waste in bioreactor landfills. Bioresour. Technol. 99, 5418–5426. Feely, R.A., Alin, S.R., Newton, J., Sabine, C.L., Warner, M., Devol, A., Krembs, C., Maloy, C., 2010. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar. Coast. Shelf Sci. 88, 442–449. Gattuso, J.P., Hansson, L., 2011. Ocean Acidification. Oxford University Press. Gilde, K., Pinckney, J.L., 2012. Sublethal effects of crude oil on the community structure of estuarine phytoplankton. Estuar. Coasts 35, 853–861. González, J., Fernández, E., Figueiras, F., Varela, M., 2013. Subtle effects of the water soluble fraction of oil spills on natural phytoplankton assemblages enclosed in mesocosms. Estuar. Coast. Shelf Sci. 124, 13–23.


González, J., Figueiras, F., Aranguren-Gassis, M., Crespo, B., Fernández, E., Morán, X.A.G., Nieto-Cid, M., 2009. Effect of a simulated oil spill on natural assemblages of marine phytoplankton enclosed in microcosms. Estuar. Coast. Shelf Sci. 83, 265–276. Götze, S., Matoo, O.B., Beniash, E., Saborowski, R., Sokolova, I.M., 2014. Interactive effects of CO2 and trace metals on the proteasome activity and cellular stress response of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Aquat. Toxicol. 149, 65–82. Hadjoudja, S., Vignoles, C., Deluchat, V., Lenain, J.F., Le Jeune, A.H., Baudu, M., 2009. Short term copper toxicity on Microcystis aeruginosa and Chlorella vulgaris using flow cytometry. Aquat. Toxicol. 94, 255–264. Hazen, T.C., Dubinsky, E.A., DeSantis, T.Z., Andersen, G.L., Piceno, Y.M., Singh, N., Jansson, J.K., Probst, A., Borglin, S.E., Fortney, J.L., et al., 2010. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330, 204–208. Hing, L.S., Ford, T., Finch, P., Crane, M., Morritt, D., 2011. Laboratory stimulation of oil-spill effects on marine phytoplankton. Aquat. Toxicol. 103, 32–37. Hirose, K., 2006. Chemical speciation of trace metals in seawater: a review. Anal. Sci. 22, 1055. Hirose, K., 2011. Chemical modeling of marine trace metals: Effects of ocean acidification to marine ecosystem, Natural Computation (ICNC). In: 2011 Seventh International Conference on IEEE, pp. 2023–2026. Hoegh-Guldberg, O., Mumby, P., Hooten, A., Steneck, R., Greenfield, P., Gomez, E., Harvell, C., Sale, P., Edwards, A., Caldeira, K., 2007. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742. Hofmann, M., Schellnhuber, H.J., 2009. Oceanic acidification affects marine carbon pump and triggers extended marine oxygen holes. Proc. Natl. Acad. Sci. USA 106, 3017–3022. Howarth, R.W., 2008. Coastal nitrogen pollution: a review of sources and trends globally and regionally. Harmful Algae 8, 14–20. Hu, X., Cai, W.J., 2013. Estuarine acidification and minimum buffer zone—a conceptual study. Geophys. Res. Lett. 40, 5176–5181. Huang, Y.J., Jiang, Z.B., Zeng, J.N., Chen, Q.Z., Zhao, Y.Q., Liao, Y.B., Shou, L., Xu, X.Q., 2011. The chronic effects of oil pollution on marine phytoplankton in a subtropical bay, China. Environ. Monit. Assess. 176, 517–530. Huesemann, M.H., Skillman, A.D., Crecelius, E.A., 2002. The inhibition of marine nitrification by ocean disposal of carbon dioxide. Mar. Pollut. Bull. 44, 142–148. Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J., Kleypas, J., 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933. Ivanina, A.V., Hawkins, C., Sokolova, I.M., 2014. Immunomodulation by the interactive effects of cadmium and hypercapnia in marine bivalves Crassostrea virginica and Mercenaria mercenaria. Fish Shellfish Immunol. 37, 299–312. Ivanina, A.V., Sokolova, I.M., 2013. Interactive effects of pH and metals on mitochondrial functions of intertidal bivalves Crassostrea virginica and Mercenaria mercenaria. Aquat. Toxicol. 144, 303–309. JiyalalRam, M.J., Ram, A., Rokade, M.A., Karangutkar, S.H., Yengal, B., Dalvi, S., Acharya, D., Sharma, S., Gajbhiye, S.N., 2013. Phytoplankton dynamic responses to oil spill in Mumbai Harbour. Int. J. Biol. Inno. Res. 2, 30–50. Jurado, E., Jaward, F., Lohmann, R., Jones, K.C., Simó, R., Dachs, J., 2005. Wet deposition of persistent organic pollutants to the global oceans. Environ. Sci. Technol. 39, 2426–2435. Kadar, E., Fisher, A., Stolpe, B., Harrison, R.M., Parello, F., Lead, J., 2012. Metallic nanoparticle enrichment at low temperature, shallow CO2seeps in Southern Italy. Mar. Chem. 140, 24–32. Keeling, R.F., Körtzinger, A., Gruber, N., 2010. Ocean deoxygenation in a warming world. Ann. Rev. Mar. Sci. 2, 199–229. Kerfahi, D., Hall-Spencer, J.M., Tripathi, B.M., Milazzo, M., Lee, J., Adams, J.M., 2014. Shallow water marine sediment bacterial community shifts along a natural CO2 gradient in the Mediterranean Sea Off Vulcano, Italy. Microbiol. Ecol. 67, 819– 828. Kvenvolden, K., Cooper, C., 2003. Natural seepage of crude oil into the marine environment. Geo-Mar. Lett. 23, 140–146. Lacoue-Labarthe, T., Martin, S., Oberhänsli, F., Teyssié, J.L., Markich, S., Jeffree, R., Bustamante, P., 2009. Effects of increased pCO2 and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences 6, 1–3. Lacoue-Labarthe, T., Reveillac, E., Oberhänsli, F., Teyssié, J.L., Jeffree, R., Gattuso, J.P., 2011. Effects of ocean acidification on trace element accumulation in the earlylife stages of squid Loligo vulgaris. Aquat. Toxicol. 105, 166–176. Lacoue-Labarthe, T., Martin, S., Oberhänsli, F., Teyssié, J.L., Jeffree, R., Gattuso, J.P., Bustamante, P., 2012. Temperature and pCO2 effect on the bioaccumulation of radionuclides and trace elements in the eggs of the common cuttlefish, Sepia officinalis. J. Exp. Mar. Biol. Ecol. 413, 45–49. Louis, Y., Garnier, C., Lenoble, V., Omanovic´, D., Mounier, S., Pizˇeta, I., 2009. Characterisation and modelling of marine dissolved organic matter interactions with major and trace cations. Mar. Environ. Res. 67, 100–107. Macdonald, R.W., Harner, T., Fyfe, J., 2005. Recent climate change in the Arctic and its impact on contaminant pathways and interpretation of temporal trend data. Sci. Total Environ. 342, 5–86. McClintock, J.B., Amsler, C.D., Amsler, M.O., Duquette, A., Angus, R.A., Hall-Spencer, J.M., Milazzo, M., 2014. Trace elements in shells of common gastropods in the near vicinity of a natural CO2 vent: no evidence of pH-dependent contamination. Biogeosciences 11, 5215–5237. Milazzo, M., Rodolfo-Metalpa, R., San Chan, V.B., Fine, M., Alessi, C., Thiyagarajan, V., Hall-Spencer, J.M., Chemello, R., 2014. Ocean acidification impairs vermetid reef recruitment. Sci. Rep. 4, 4189, 10-1038/srep04189.

Please cite this article in press as: Zeng, X., et al. The positive relationship between ocean acidification and pollution. Mar. Pollut. Bull. (2014), http://


X. Zeng et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Millero, F.J., 2009. Effect of ocean acidificationon the speciation of metals in seawater. Oceanography 22, 72–85. Morel, F., Milligan, A., Saito, M., 2006. The Oceans and Marine Geochemistry, vol. 6. Elsevier, pp. 113–143. Mostofa, K.M., Liu, C.Q., Vione, D., Gao, K., Ogawa, H., 2013. Sources, factors, mechanisms and possible solutions to pollutants in marine ecosystems. Environ. Pollut. 182, 461–478. Mucci, A., Starr, M., Gilbert, D., Sundby, B., 2011. Acidification of lower St. Lawrence estuary bottom waters. Atmosphere-Ocean 49, 206–218. Nikinmaa, M., 2013. Climate change and ocean acidification – interactions with aquatic toxicology. Aquat. Toxicol. 126, 365–372. Olaniran, A.O., Balgobind, A., Pillay, B., 2011. Quantitative assessment of the toxic effects of heavy metals on 1,2-dichloroethane biodegradation in cocontaminated soil under aerobic condition. Chemosphere 85, 839–847. Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681– 686. Ozhan, K., Bargu, S., 2014. Distinct responses of Gulf of Mexico phytoplankton communities to crude oil and the dispersant corexitÒ Ec9500A under different nutrient regimes. Ecotoxicology, 1–15. Pandolfi, J.M., Connolly, S.R., Marshall, D.J., Cohen, A.L., 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422. Pascal, P.Y., Fleeger, J.W., Galvez, F., Carman, K.R., 2010. The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. Mar. Pollut. Bull. 60, 2201–2208. Rabalais, N.N., Cai, W.J., Carstensen, J., Conley, D.J., Fry, B., Hu, X., Quinones-Rivera, Z., Rosenberg, R., Slomp, C.P., Turner, R.E., 2014. Eutrophication-driven deoxygenation in the coastal ocean. Oceanography 27, 172–183. Richards, R., Chaloupka, M., Sano, M., Tomlinson, R., 2011. Modelling the effects of ‘coastal’ acidification on copper speciation. Ecol. Mod. 222, 3559–3567. Riebesell, U., Gattuso, J.P., Thingstad, T.F., Middelburg, J., 2013. Arctic Ocean acidification: pelagic ecosystem and biogeochemical responses during a mesocosm study. Biogeosciences 10, 5619–5626. Roberts, D.A., Birchenough, S.N., Lewis, C., Sanders, M.B., Bolam, T., Sheahan, D., 2013. Ocean acidification increases the toxicity of contaminated sediments. Global Change Biol. 19, 340–351. Rue, E.L., Bruland, K.W., 1995. Complexation of iron (III) by natural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method. Mar. Chem. 50, 117–138. Saito, M.A., Rocap, G., Moffett, J.W., 2005. Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol. Oceanogr. 50, 279–290.

Sandrin, T.R., Maier, R.M., 2003. Impact of metals on the biodegradation of organic pollutants. Environ. Health Perspect. 111, 1093–1101. Santos, E.C., Jacques, R.J., Bento, F.M., Peralba, M.d.C.R., Selbach, P.A., Sá, E.L., Camargo, F.A., 2008. Anthracene biodegradation and surface activity by an ironstimulated Pseudomonas sp.. Bioresour. Technol. 99, 2644–2649. Shi, D., Kranz, S.A., Kim, J.M., Morel, F.M., 2012. Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under lowiron conditions. Proc. Natl. Acad. Sci. USA 109, E3094–E3100. Shi, D., Xu, Y., Hopkinson, B.M., Morel, F.M., 2010. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327, 676–679. Slomp, C.P., 2011. Marine pollution: give more priority to phosphorus studies. Nature 478, 459–459. Sunda, W.G., Cai, W.J., 2012. Eutrophication induced CO2-acidification of subsurface coastal waters: interactive effects of temperature, salinity, and atmospheric pCO2. Environ. Sci. Technol. 46, 10651–10659. Torres, M.A., Barros, M.P., Campos, S.C., Pinto, E., Rajamani, S., Sayre, R.T., Colepicolo, P., 2008. Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol. Environ. Saf. 71, 1–15. Vizzini, S., Di Leonardo, R., Costa, V., Tramati, C.D., Luzzu, F., Mazzola, A., 2013. Trace element bias in the use of CO2 vents as analogues for low pH environments: implications for contamination levels in acidified oceans. Estuar. Coast. Shelf Sci. 134, 19–30. Waldbusser, G.G., Salisbury, J.E., 2014. Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains, and habitats. Ann. Rev. Mar. Sci. 6, 221–247. Waldbusser, G.G., Voigt, E.P., Bergschneider, H., Green, M.A., Newell, R.I., 2011. Biocalcification in the eastern oyster (Crassostrea virginica) in relation to longterm trends in Chesapeake Bay pH. Estuar. Coasts 34, 221–231. Wang, L., Zheng, B., 2008. Toxic effects of fluoranthene and copper on marine diatom Phaeodactylum tricornutum. J. Environ. Sci (China) 20, 1363–1372. Wang, M.J., Wang, W.X., 2009. Cadmium in three marine phytoplankton: accumulation, subcellular fate and thiol induction. Aquat. Toxicol. 95, 99–107. Wu, Y., Wang, W.X., 2011. Accumulation, subcellular distribution and toxicity of inorganic mercury and methylmercury in marine phytoplankton. Environ. Pollut. 159, 3097–3105. Wu, Y., Wang, W.X., 2014. Intracellular speciation and transformation of inorganic mercury in marine phytoplankton. Aquat. Toxicol. 148, 122–129. Xiong, B., Zhang, W., Chen, L., Lin, K.F., Guo, M.J., Wang, W.L., Cui, X.H., Bi, H.S., Wang, B., 2013. Effects of Pb (II) exposure on chlorella protothecoides and chlorella vulgaris growth, malondialdehyde, and photosynthesis-related gene transcription. Environ. Toxicol. 29, 1346–1354. Xu, Y., Shi, D., Aristilde, L., Morel, F.M., 2012. The effect of pH on the uptake of zinc and cadmium in marine phytoplankton: possible role of weak complexes. Limnol. Oceanogr. 57, 293–304.

Please cite this article in press as: Zeng, X., et al. The positive relationship between ocean acidification and pollution. Mar. Pollut. Bull. (2014), http://

The positive relationship between ocean acidification and pollution.

Ocean acidification and pollution coexist to exert combined effects on the functions and services of marine ecosystems. Ocean acidification can increa...
786KB Sizes 6 Downloads 11 Views