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Estuarine, Coastal and Shelf Science 148 (2014) 1e13
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Coastal ocean acidiﬁcation: The other eutrophication problem Ryan B. Wallace a, Hannes Baumann a, Jason S. Grear b, Robert C. Aller a, Christopher J. Gobler a, * a
Stony Brook University, School of Marine and Atmospheric Sciences, 239 Montauk Hwy, Southampton, NY 11968, USA US Environmental Protection Agency, Atlantic Ecology Division, National Health and Environmental Effects Research Laboratory, Ofﬁce of Research and Development, 27 Tarzwell Dr, Narragansett, RI 02882, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 8 March 2014 Accepted 26 May 2014 Available online 5 June 2014
Increased nutrient loading into estuaries causes the accumulation of algal biomass, and microbial degradation of this organic matter decreases oxygen levels and contributes towards hypoxia. A second, often overlooked consequence of microbial degradation of organic matter is the production of carbon dioxide (CO2) and a lowering of seawater pH. To assess the potential for acidiﬁcation in eutrophic estuaries, the levels of dissolved oxygen (DO), pH, the partial pressure of carbon dioxide (pCO2), and the saturation state for aragonite (Uaragonite) were horizontally and vertically assessed during the onset, peak, and demise of low oxygen conditions in systems across the northeast US including Narragansett Bay (RI), Long Island Sound (CTeNY), Jamaica Bay (NY), and Hempstead Bay (NY). Low pH conditions (3000 matm), were acidic pH (300 million liters per day of treated wastewater efﬂuent, and ended within the inlet to the Atlantic Ocean. Maps of continually measured levels of DO and pCO2 were generated using ArcGIS 10 (ESRI, Redlands, CA). 3. Results Over an annual cycle, levels of pHNBS and DO were strongly coupled and highly dynamic within the western extent of LIS, particularly within bottom waters where peak levels of pHNBS (8.76) and DO (11.83 mg L1) occurred in winter coincident with the winterespring bloom and minimal values of 7.23 and 0.94 mg L1, respectively, occurred during summer (Fig. 2A). Similar temporal patterns occurred within surface waters of western LIS, although the values were less extreme with pHNBS ranging from 8.32 in winter to 7.48 in summer and DO ranging from 13.1 mg L1 in winter to 5.33 mg L1 during summer (Fig. 2B). Within eastern LIS, similar temporal patterns were observed for DO, although the range in values was smaller for bottom (4.86e11.5 mg L1; Fig. 2C) and surface waters (6.43e11.7 mg L1; Fig. 2D) compared to western LIS. pHNBS within eastern LIS also had a smaller dynamic range (7.43e8.57), was similar between surface and bottom waters, and displayed a less distinct seasonal pattern. A cross sectional examination of chlorophyll a, pH and DO in LIS revealed the vertical, horizontal, and temporal evolution of phytoplankton biomass, hypoxia, and acidiﬁcation in this system.
Fig. 2. Time series of DO and pHNBS, August, 2010eOctober, 2012. A) Western Long Island Sound, bottom & B) surface. C) Eastern Long Island Sound, bottom & D) surface.
While oxygen and pH levels were normal throughout the water column in LIS during May (pHNBS > 8; DO > 7.5 mg L1; Fig. 3), these conditions changed with the onset of summer. Speciﬁcally, pH levels were lower throughout LIS in June, while DO levels began to decline in western bottom waters (Fig. 3). During July, August, and September, hypoxic and acidiﬁed conditions were present in western LIS as DO levels declined to 7.9 and >7.5 mg L1, respectively (Fig. 3). Given the co-occurrence of hypoxia and acidiﬁcation in western LIS during August of 2010 and 2011, a cruise focusing on the western half of LIS was performed to assess the levels of pCO2 and Uaragonite present in August 2012. While the surface mixed layer of eastern LIS had elevated levels of pHT and DO (>7.7, >7 mg L1), moderate pCO2 levels (~500 matm), and was saturated with respect to aragonite (Uaragonite > 1; Fig. 4), these conditions deteriorated signiﬁcantly to the west, particularly within bottom waters. Speciﬁcally, nearly all bottom waters of LIS had pHT values 1000 matm; Uaragonite < 1; Fig. 5). Like many river fed estuaries, Narragansett Bay exhibits a stronger vertical salinity gradient than LIS, particularly within its northern extent. Regardless, the two systems displayed similar horizontal and vertical gradients of DO, pH, pCO2, and Uaragonite during summer months. For example, in June much of the water column within the northern, lower salinity region of the Bay had low DO (4000 matme~500 matm, while DO levels increased in parallel from 7 mg L1), bottom waters across the entire bay displayed signs of acidiﬁcation with pHT < 7.7, pCO2 >1000 matm, and Uaragonite < 1.5 (Fig. 6). During July and August, this acidiﬁcation pattern persisted in Narragansett Bay with values of pHT, pCO2, and Uaragonite being similar to June, whereas DO levels across the southern extent of Bay declined in July (3000 matm pCO2 and acidic seawater (pH < 7.0). Summer changes in temperature account for 7.7; DO > 5 mg L1). Similarly, within Narragansett Bay and Jamaica Bay, the regions of the estuaries with the most intense algal blooms and highest nutrient concentrations (Supplementary Figs. 2 and 3) were the same regions that experienced the lowest levels of pH and DO during our study.
Fig. 6. Monthly vertical section plots of DO (measured via a YSI 6450 optical DO sensor), pHT (measured via a Durafet III pH sensor), pCO2 and UAragonite (both calculated from discrete measurements of DIC and pH via a Durafet III sensor) with salinity (measured via a YSI 6920 V2) contour lines during the summer of 2013 in Narragansett Bay. Vertical lines indicate CTD proﬁles. Depth is 0e15 m.
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Fig. 7. Monthly vertical section plots of DO (measured via a YSI 6450 optical DO sensor), pHT (measured via a SeaFET pH sensor) and pCO2 (measured via a HydroC CO2 sensor) during August, September, and November of 2012 in Jamaica Bay. During the August and November cruises temperature stratiﬁcation was not observed (25 C and 6 C, respectively) and contours are not included whereas September contour lines are temperature ( C, measured via a YSI 6920 V2). Vertical lines indicate CTD proﬁles. Depth is 0e15 m.
At a fundamental level eutrophication is commonly associated with enhanced nutrient loading that stimulates phytoplankton blooms (Nixon 1995) and, via photosynthesis, should consume CO2 and increase pH levels. Indeed, our analysis of annual pH cycles in LIS demonstrated that the winterespring phytoplankton bloom period was associated with highly basic pH values (>8.5; Fig. 2). These peak pH values, usually during February in LIS and other systems (Baumann et al., 2014), are followed by a progressive decline in pH by more than one unit to < 7.5 during summer and fall as microbial respiration rates intensify. Therefore, while eutrophication does promote algal blooms that can raise the pH and DO of surface waters in winter, the remineralization of this algal organic matter during summer and fall leads to the seasonal acidiﬁcation
detected in all four study sites, particularly in bottom waters. Furthermore, in stratiﬁed, deeper systems (LIS, Narragansett Bay), there can be a spatial decoupling of productivity, hypoxia, and acidiﬁcation with high productivity conﬁned to surface layers, and low DO and pH found extensively across bottom waters. In other cases, however, strong summer hypoxia and acidiﬁcation existed in the presence of elevated levels of algal biomass (e.g. Fig. 3, western LIS in September 2011; Fig. 7, Jamaica Bay in August 2012). While comprehensive surveys of pH and pCO2 within estuaries are not common, some preliminary hypotheses can be developed regarding the types of systems that may be the most prone to acidiﬁcation based on this and prior studies. Measurements of ecosystem metabolism within 42 US estuaries demonstrated that
Fig. 8. Horizontal cruise tracks across Jamaica Bay during early November, 2011 of A) surface pCO2 (measured via a HydroC CO2 sensor) and B) DO (measured via a YSI 6450 optical DO sensor) with associated correlations between C) salinity & pCO2 and D) DO & pCO2.
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Fig. 9. Surface pCO2 levels in Hempstead Bay as measured via a HydroC CO2 sensor during a cruise conducted in late October, 2011. Levels of pCO2 > 700 matm are within close proximity (3 km) of a sewage treatment plant outfall.
93% were net heterotrophic, experiencing an annual net consumption of DO (Caffrey, 2004) and thus production of pCO2 and likely some degree of seasonal acidiﬁcation. Among the 20 salt marsh-dominated estuaries surveyed by Caffrey (2004), all were net heterotrophic. Salt marshes host extreme levels of microbial metabolism (Dame et al., 1986; Koch and Gobler, 2009) and the two lagoons studied here (Jamaica and Hempstead Bay) have signiﬁcant stands of salt marsh. As such, beyond eutrophication-driven acidiﬁcation, salt marshes may have also promoted the high pCO2 conditions in these shallow systems. Our recent 5-yr study of another NY salt marsh (Flax Pond) found a highly signiﬁcant correlation between DO and pH and extreme acidiﬁcation in summer, particularly during low tides and at night (pCO2 >4000 matm; Baumann et al., 2014). Conversely, high rates of autotrophy make seagrass meadows a signiﬁcant sink for carbon (Duarte et al., 2010). Accordingly, seagrass-dominated estuaries, which must be shallow to host such benthic vegetation, are often net autotrophic (Caffrey, 2004) and are likely to buffer against ocean acidiﬁcation in the water column (Hendriks et al., 2014). Beyond the photosynthetic activity of the submerged aquatic vegetation, shallow estuaries are also more likely to be well-mixed, rapidly equilibrating with atmospheric CO2, and thus may be generally less vulnerable to continued respiratory acidiﬁcation than deeper systems (such as LIS) that are typically stratiﬁed in summer and have a smaller fraction of the water column within the euphotic zone. These shallow systems may, however, be vulnerable to large diurnal variations in pH and DO particularly in cases of excessive loadings of organic matter (Baumann et al., 2014). Shallow estuaries are more responsive to nutrient loading and often shift from net autotrophic to net heterotrophic on diel timescales with the intensity of these shifts linked to the intensity of nutrient loading (O'Boyle et al., 2013). Given that all of the surveys presented here occurred during the day, the extent of acidiﬁcation in some of these systems is likely even more extreme at night, particularly within shallow regions. Finally, extended residence times within estuaries are likely to exacerbate acidiﬁcation as poorly ﬂushed waters will be more likely to accumulate pCO2 during periods of intense organic matter remineralization. Coastal acidiﬁcation in the US has been most commonly examined along the Paciﬁc coast where deep, pCO2-enriched waters are seasonally upwelled (Feely et al., 2008, 2010; Hofmann et al., 2011) and negatively impact oyster populations in
hatcheries (Barton et al., 2012) and in the wild (Hettinger et al., 2013). In contrast, the enclosed, eutrophic estuaries, with extended residence times and strong summer hypoxia such as those studied here are similar to other systems across the US East Coast (e.g. Chesapeake Bay; Kemp et al., 2005), in Europe (e.g. Baltic Sea; Melzner et al., 2013; Sunda and Cai, 2012), and southeast Asia (e.g. Yangtze Estuary; Chen et al., 2007). Given the widespread nature of hypoxia around the globe (Diaz and Rosenberg, 2008), it would seem that eutrophication-induced acidiﬁcation may currently be a more common phenomenon than the upwellinginduced acidiﬁcation that occurs on the US West Coast. Clearly, more studies of coastal ocean acidiﬁcation will be required to evaluate this hypothesis. Finally, the acidiﬁcation detected during this study is likely conﬁned to estuaries, as recent large scale surveys of the US Gulf and East Coasts determined that well-mixed shelf waters from Texas to Maine were supersaturated with respect to aragonite during summer (Wang et al., 2013). That same study also found, however, that the shelf waters of the northeast US had substantially lower pH and buffering capacity than all other regions surveyed and inferred that this region is more susceptible to acidiﬁcation than other parts of the US Gulf and East coasts (Wang et al., 2013), a hypothesis consistent with the ﬁnding of the present study. While hypoxia and acidiﬁcation co-occurred in estuaries during summer, some observations suggest low pH conditions may persist longer into the fall than low oxygen. For example, during 2011 and 2013 in LIS and during 2012 in Jamaica Bay, waters transitioned from hypoxic to normoxic during early fall (October) but maintained pHT levels < 7.7. These differences may be a function of the differential diffusion and solubility of O2 and CO2 as a function of temperature (Millero et al., 2006). Cooler fall temperatures enhance gas solubility, and may contribute toward a more extended period of acidiﬁcation during fall compared to hypoxia, even in the face of slowing microbial respiration. In the case of DO, cooler temperatures will lead to a diffusion of oxygen into water whereas in the case of CO2, cooler temperatures will slow the diffusion out of water. An additional factor that likely enhances acid production (lower pH) during times when DO levels are increasing is the oxidation of anaerobic metabolites. The reduced constituents (e.g., 2þ 2þ NHþ 4 , HS , Fe , Mn ) that build up in surface sediments during hypoxia oxidize seasonally when systems re-oxygenate (Soetaert et al., 2007). These oxidation reactions produce strong acids that titrate alkalinity, lower pH, and could promote shell dissolution in bivalves (Green and Aller 1998). As such, the seasonal duration of acidiﬁcation as a selective pressure in estuarine organisms may be longer than the seasonal pressures imposed by hypoxia. Beyond microbial respiration driven by internal, autochtonous sources of organic carbon, this study provides evidence that the discharge of wastewater from sewage treatment plants is a previously unappreciated, point source of acidiﬁcation and high pCO2 water in coastal zones. While these low pH conditions may be partly a function of microbial respiration of the allochthonous organic matter discharged from sewage within the estuary, it is also likely the discharged sewage itself is acidiﬁed. This was most obvious during our horizontal cruises across the lagoons in southwest Long Island where a radius of several kilometers of estuarine surface waters around sewage outfall sites had levels of pCO2 near or above 1000 matm (several times supersaturated). The surface waters of western LIS are highly enriched in wastewater (Sweeney and Sanudo-Wilhelmy, 2004) and had surface waters with nearly the same low pH and high pCO2 as bottom waters during summer and fall. Due to its high organic matter load, wastewater experiences extreme amounts of microbial respiration and has been previously shown to be low in pH (6e8) and DO (at times anoxic) and enriched in pCO2 (Gallert and Winter, 2005). A management
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goal for LIS (USEPA, 1994) and other coastal systems is to remove N from wastewater to relieve the symptoms of eutrophication including hypoxia (Nixon and Buckley, 2002). Given that the removal of N is generally achieved via increased microbial activity (i.e. biological denitriﬁcation), this enhanced level of N removal may yield efﬂuent with lower pH and high pCO2 levels (Soetaert et al., 2007). As such, it is possible that coastal regions in close proximity to wastewater discharge may experience more intense acidiﬁcation as treatment plants are upgraded with higher amounts of denitriﬁcation to alleviate other symptoms of eutrophication. Given the chronically high concentrations of pCO2 in regions within close proximity to sewage treatment plant discharge (>1000 matm), it seems likely that these sites may have a localized impact on the surrounding ﬂora and fauna in a manner that parallels other concentrated sources of pCO2 including volcanic seeps (Fabricius et al., 2011). The connection between eutrophication and acidiﬁcation was further evidenced by the relationship between DO and pH for the three major systems studied here: LIS, Narragansett Bay, and Jamaica Bay (Fig. 10). For all of the sites, there was a highly signiﬁcant, linear relationship between DO and pH (p < 0.0001), with Jamaica Bay displaying the strongest relationship (R ¼ 0.94) and LIS showing more variance (R ¼ 0.70). The correlation for Jamaica Bay was slightly improved with a logarithmic ﬁt (R ¼ 0.94). This variability in LIS was partly a function of the depth of this system as during summer, stratiﬁed conditions, DO levels were largely uniform below the mixed layer, while pH levels continued to decline to the bottom. General linear regression models of the DO-pH relationship for each system provided y-intercept values for Jamaica Bay, LIS, and Narragansett Bay of 7.07, 7.14, and 7.25, respectively, representing the levels of pHT predicted under anoxic conditions (DO ¼ 0; Fig. 10). These values further emphasize linkages between eutrophication and acidiﬁcation. Jamaica Bay receives ~90% of its N load from sewage discharge (Benotti et al., 2007) and is predicted to experience the most extreme acidiﬁcation under anoxic conditions (pHT ¼ 7.07). In contrast, Narragansett Bay experiences excessive nutrient loading within its northern extent, but is a more oligotrophic system to the south (Nixon et al., 2008), and was predicted to experience the highest pHT under anoxic conditions (7.25). LIS was similar to Jamaica Bay (anoxic pHT ¼ 7.14), but was not as extreme, again likely reﬂecting the more hybrid nature of this
Fig. 10. All paired measurements (n ¼ 6652) of surface pHT and DO from LIS, Jamaica Bay, and Narragansett Bay. General linear regression models for each site yielded equations and correlation coefﬁcients of y ¼ 0.084x þ 7.06, R ¼ 0.94 for Jamaica Bay, y ¼ 0.081x þ 7.25, R ¼ 0.84 for Narragansett Bay, and y ¼ 0.085x þ 7.14, R ¼ 0.70 for LIS.
system: While its western extreme receives large nutrient inputs from NYC (Parker and O’Reilly, 1991; O’Shea and Bronsan, 2000) and can be acidic (pH < 7), the eastern end exchanges with the Atlantic Ocean and is fairly oligotrophic (Gobler et al., 2006). 4.2. Biological implications This study establishes that estuarine pelagic organisms in temperate zones are commonly exposed to acidiﬁcation and waters undersaturated with regard to aragonite during summer and fall months. Consistent with our study, Feely et al. (2010) reported that most of Puget Sound, WA, USA, was undersaturated with regard to aragonite during August. The summer levels of pH, pCO2, and calculated Uaragonite present through large areas within the estuaries studied here during summer (pH < 7.7T, pCO2 > 1000 matm, Uaragonite < 1) are within the range that have been shown in laboratory studies to reduce the growth and survival of early life stage mollusks (Gazeau et al., 2013) and ﬁsh (Baumann et al., 2012; Frommel et al., 2012; Chambers et al., 2013). Furthermore, these conditions emerge at the same times that many mollusks and ﬁsh spawn in estuaries (Kennedy and Krantz, 1982; Bricelj et al., 1987; Able and Fahay, 1998; Kraeuter and Castagna, 2001), suggesting that some early life stage ﬁsh and mollusks sensitive to acidiﬁcation may be negatively impacted by high levels of pCO2 and low levels of pH and carbonate. Therefore, we suggest that acidiﬁcation should be considered among the factors that shape ﬁsheries yields in coastal zones. A vivid example of this may be the bay scallop (Argopecten irradians) which is known to spawn in mid-to-late summer (July, August) and is one of the organisms most sensitive to acidiﬁcation (Talmage and Gobler, 2009, 2010, 2011), experiencing signiﬁcant declines in survival when exposed to pCO2 750 matm for only four days (Gobler and Talmage, 2013). While the collapse of this ﬁshery in NY waters was caused by toxic algae blooms decades ago (Gobler et al., 2005), the failure of this population to recover despite signiﬁcant restoration efforts may be caused, at least in part, by the overlap of annual spawning events with acidiﬁed conditions in estuaries. We note that during this and prior studies (Baumann et al., 2014), there has been signiﬁcant interannual variation in the intensity and timing of acidiﬁcation with warmer spring and summers being associated with earlier onset and more intense acidiﬁcation (e.g. during 2012; this study; Baumann et al., 2014). If the impaired traits are indeed important to the ﬁtness of commercially viable species, then such interannual changes in the timing and intensity of acidiﬁcation may inﬂuence the annual yields of some ﬁsheries such as bay scallops. While there is great variability in biological response to acidiﬁcation among species (Kroeker et al., 2010, 2013) the ecosystem level effects will depend on the extent to which sensitive species or functional groups govern critical ecological processes (e.g ﬁlter feeding by calcifying bivalves). The effects of acidiﬁcation on marine life will partly be a function of differences between exposure levels for benthic and pelagic organisms as well as the differential susceptibility and demographic importance of various life stages. During this study, bottom waters were always more acidiﬁed than surface waters suggesting benthic organisms are subject to more extended periods of dissolution (Green and Aller, 1998) and need to be more tolerant of acidiﬁcation than pelagic species (Waldbusser and Salisbury 2014). Regarding bivalves, larval stages which are generally pelagic are known to be more sensitive to acidiﬁcation than benthic, juvenile stages (Talmage and Gobler, 2011; Gazeau et al., 2013). While larval stages are spared intense levels of acidiﬁcation near or in the benthos (Green et al., 1998), in highly eutrophic systems during summer (e.g. western LIS and Jamaica Bay), the entire water column was undersaturated with regard to aragonite,
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suggesting even pelagic species and life stages will be exposed to conditions unfavorable for calciﬁcation. We commonly observed pCO2 > 1000 matm in bottom waters during summer months, with the most eutrophic estuarine regions exhibiting >3000 matm pCO2 and acidic seawater (pH < 7.0). These observations demonstrate that the recommendation to restrict ocean acidiﬁcation experiments with marine organisms to pCO2 levels of 1000 matm and below to mimic future climate change (Riebesell et al., 2010) should be heeded for open ocean species only. Indeed, given that estuarine organisms persisting within deeper regions of the systems studied here may rarely experience pCO2 below 1000 matm during summer months, experiments designed to assess the realistic effects of current and future acidiﬁcation on coastal species will need to target pCO2 levels signiﬁcantly beyond 1000 matm. In addition to acidiﬁcation, this study further demonstrates the well-known tenet that estuarine organisms are often challenged by the stress of hypoxia during summer (Rabalais et al., 2002; Diaz and Rosenberg, 2008). Furthermore, in some cases, estuarine organisms already existing near their upper temperature threshold may € rtner 2008, 2010). Hence, experience concurrent thermal stress (Po it would seem the ‘hot, sour, and breathless’ (high temperature, low pH, low DO) conditions predicted for the future open ocean (Gruber et al., 2011) can already be found in today's coastal zones during summer, and especially within the benthos where pH and DO levels are generally lower than the water column (Zhu et al., 2006). Prior research has demonstrated that each of these stressors individually creates a signiﬁcant physiological challenge to marine organisms and that their co-occurrence can have complex, interactive effects €rtner 2008, 2010). Several recent studies on their performance (Po have examined the manner in which elevated temperatures and ocean acidiﬁcation impact ocean organisms (Talmage and Gobler, 2011; Hiebenthal et al., 2013; Byrne and Przeslawski, 2013). In contrast, the concurrent effects of low oxygen and acidiﬁcation on marine animals are largely unknown, as most prior studies of hypoxia and thermal stress have not considered concurrent low pH levels. Recently, it has been discovered that hypoxia and acidiﬁcation can have additive and synergistic negative effects on the growth, survival, and metamorphosis of early life stage bivalves (Gobler et al., 2014). Given this ﬁnding and the frequency of low pH and low DO waters in estuaries (Cai et al., 2011; Sunda and Cai, 2012; Melzner et al., 2013; this study), a comprehensive assessment of the effects of hypoxia and acidiﬁcation on marine life is needed to understand how coastal ecosystems will respond to these conditions both today and under future climate change scenarios. 4.3. Management implications The revelation that water column acidiﬁcation can be intense and widespread in estuaries may have important management implications. In light of the threat of hypoxia to ﬁsheries and biodiversity (Gray et al., 2002; Levin et al., 2009), coastal management agencies often set criteria for dissolved oxygen based on levels known to be harmful to estuarine organisms (Vaquer-Sunyer and Duarte, 2008; USEPA 2000). Given that the levels of pH detected during this study have been shown to be harmful to several forms of marine life (Talmage and Gobler, 2009; Baumann et al., 2012; Gazaeu et al., 2013) and that concurrent acidiﬁcation and low oxygen can synergistically depress survival rates of bivalves (Gobler et al., 2014), managerial criteria based strictly on DO may not protect estuarine animals as anticipated. While signiﬁcantly more research is needed to better understand the co-effects of hypoxia and acidiﬁcation on estuarine organisms, future environmental regulations developed to protect coastal organisms in
regions prone to hypoxia should consider the concurrent effects of acidiﬁcation on these animals. Further, nutrient management plans in acidiﬁed estuaries may consider the level of nutrient load reduction required to alleviate low pH conditions and the associated impacts on marine life. Finally, given that rising atmospheric CO2 levels will further depress estuarine pH levels (Miller et al., 2009), the importance of management efforts that address coastal acidiﬁcation will continue to increase through this century. Acknowledgments This research was supported by NOAA's Ocean Acidiﬁcation Program through award #NA12NOS4780148 from the National Centers for Coastal Ocean Science, the National Science Foundation (NSF # 1129622), and the Chicago Community Trust. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.ecss.2014.05.027. References Able, K.W., Fahay, M.P., 1998. The First Year in the Life of Estuarine Fishes in the Middle Atlantic Bight. Rutgers University Press. Anderson, T.H., Taylor, G.T., 2001. Nutrient pulses, plankton blooms, and seasonal hypoxia in western Long Island Sound. Estuaries 24, 228e243. Barton, A., Hales, B., Waldbusser, G.G., Langdon, C., Feely, R.A., 2012. The Paciﬁc oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: Implications for near-term ocean acidiﬁcation effects. Limnol. Oceanogr. 57, 698e710. Baumann, H., Talmage, S.C., Gobler, C.J., 2012. Reduced early life growth and survival in a ﬁsh in direct response to increased carbon dioxide. Nat. Clim. Chang. 2, 38e41. Baumann, H., Wallace, R., Tagliaferri, T., Gobler, C., 2014. Large natural pH, CO2 and O2 ﬂuctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuar. Coasts. http://dx.doi.org/10.1007/s12237-12014-19800y (in press). Benotti, M.J., Abbene, M., Terracciano, S.A., 2007. Nitrogen Loading in Jamaica Bay, Long Island, New York: Predevelopment to 2005, Scientiﬁc Investigations Report. USGS. Bricelj, V.M., Epp, J., Malouf, R.E., 1987. Intraspeciﬁc variation in reproductive and somatic growth cycles of bay scallops Argopecten irradians. Mar. Ecol. Prog. Ser. 36, 123e137. Byrne, M., Przeslawski, R., 2013. Multistressor Impacts of warming and acidiﬁcation of the ocean on Marine Invertebrates' life Histories. Integr. Comp. Biol. 53, 582e596. Caffrey, J.M., 2004. Factors controlling net ecosystem metabolism in US estuaries. Estuaries 27, 90e101. Cai, W.J., Hu, X.P., Huang, W.J., Murrell, M.C., Lehrter, J.C., Lohrenz, S.E., Chou, W.C., Zhai, W.D., Hollibaugh, J.T., Wang, Y.C., Zhao, P.S., Guo, X.H., Gundersen, K., Dai, M.H., Gong, G.C., 2011. Acidiﬁcation of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766e770. Caldeira, K., Wickett, M.E., 2003. Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365. Chambers, R.C., Candelmo, A.C., Habeck, E.A., Poach, M.E., Wieczorek, D., Cooper, K.R., Greenﬁeld, C.E., Phelan, B.A., 2013. Ocean acidiﬁcation effects in the early life-stages of summer ﬂounder, Paralichthys dentatus. Biogeosci. Discuss. 10, 13897e13929. Chen, C.C., Gong, G.C., Shiah, F.K., 2007. Hypoxia in the East China Sea: one of the largest coastal low-oxygen areas in the world. Mar. Environ. Res. 64, 399e408. Cloern, J.E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 210, 223e253. Costanza, R., dArge, R., deGroot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., Oneill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., vandenBelt, M., 1997. The value of the world's ecosystem services and natural capital. Nature 387, 253e260. Dame, R., Chrzanowski, T., Bildstein, K., Kjerfve, B., McKellar, H., Nelson, D., Spurrier, J., Stancyk, S., Stevenson, H., Vernberg, J., Zingmark, R., 1986. The outwelling hypothesis and North Inlet, South Carolina. Mar. Ecol. Prog. Ser. 33, 217e229. de Jonge, V.N., Elliott, M., Orive, E., 2002. Causes, historical development, effects and future challenges of a common environmental problem: eutrophication. Hydrobiologia 475, 1e19. Diaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosystems. Science 321, 926e929. Dickson, A.G., Sabine, C.L., Christian, J.R., 2007. Guide to best practices for ocean CO2 measurements. PICES Spec. Publ. 3, 191.
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