Estuarine, Coastal and Shelf Science 148 (2014) 1e13

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Estuarine, Coastal and Shelf Science

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Invited feature Coastal acidification: The other 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 b 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 article info abstract

Article history: Increased nutrient loading into causes the accumulation of algal biomass, and microbial Received 8 March 2014 degradation of this organic matter decreases oxygen levels and contributes towards hypoxia. A second, Accepted 26 May 2014 often overlooked consequence of microbial degradation of organic matter is the production of carbon Available online 5 June 2014 dioxide (CO2) and a lowering of seawater pH. To assess the potential for acidification in eutrophic es- tuaries, the levels of dissolved oxygen (DO), pH, the partial pressure of carbon dioxide (pCO2), and the Keywords: saturation state for aragonite (Uaragonite) were horizontally and vertically assessed during the onset, peak, acidification and demise of low oxygen conditions in systems across the northeast US including Narragansett Bay (RI), pH e < estuary Long Island Sound (CT NY), Jamaica Bay (NY), and Hempstead Bay (NY). Low pH conditions ( 7.4) were hypoxia detected in all systems during summer and fall months concurrent with the decline in DO concentra- calcium carbonate saturation tions. While hypoxic waters and/or regions in close proximity to sewage discharge had extremely high respiration levels of pCO2,(>3000 matm), were acidic pH (<7.0), and were undersaturated with regard to aragonite (Uaragonite < 1), even near-normoxic but eutrophic regions of these estuaries were often relatively acidified (pH < 7.7) during late summer and/or early fall. The close spatial and temporal correspondence between DO and pH and the occurrence of extremes in these conditions in regions with the most intense nutrient loading indicated that they were primarily driven by microbial respiration. Given that coastal acidification is promoted by nutrient-enhanced organic matter loading and reaches levels that have previously been shown to negatively impact the growth and survival of marine organisms, it may be considered an additional symptom of eutrophication that warrants managerial attention. © 2014 Elsevier Ltd. All rights reserved.

1. Introduction has contributed to a significant expansion in hypoxic zones across the globe (Rabalais et al., 2002; Diaz and Rosenberg, 2008). Because Coastal marine ecosystems are amongst the most ecologically these hypoxic zones can be lethal to aerobic marine organisms and and economically productive areas on the planet, providing more have contributed toward declining yields of fisheries (Vaquer- than US$10 trillion in annual resources or ~40% of the global Sunyer and Duarte, 2008; Levin et al., 2009), a prime motivation ecosystem goods and services (Costanza et al., 1997). Approxi- of coastal zone management has been to lower nutrient loads in mately 40% of the World population lives within 100 km of a order to reduce the intensity, extent, and duration of hypoxia coastline, making these regions subject to a suite of anthropogenic (Scavia et al., 2004; Paerl, 2006; Scavia and Bricker, 2006). stressors including intense nutrient loading (de Jonge et al., 2002; A second, often overlooked consequence of microbial degrada- Valiela, 2006). Excessive nutrient loading into coastal ecosystems tion of organic matter in coastal zones is the production of CO2, promotes algal productivity and the subsequent microbial con- which enters the water and forms carbonic acid (H2CO3) dissoci- 2 sumption of this organic matter reduces oxygen levels and can ating into bicarbonate ions (HCO3 ), carbonate ions (CO3 ) and þ promote hypoxia (Cloern, 2001; Heisler et al., 2008). The rapid hydrogen ions (H ) that cause acidification. Coastal ecosystems can acceleration of nutrient loading to coastal zones in recent decades also be acidified via atmospheric carbon dioxide fluxes (Miller et al., 2009; Feely et al., 2010), the introduction of acidic river water (Salisbury et al., 2008), and/or upwelling of CO2 enriched deep * Corresponding author. water (Feely et al., 2008). Watershed geology, climate and acid E-mail address: [email protected] (C.J. Gobler). deposition also have the potential to impact source water buffering http://dx.doi.org/10.1016/j.ecss.2014.05.027 0272-7714/© 2014 Elsevier Ltd. All rights reserved. 2 R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 capacities through their effects on mineral weathering and sea ice were conducted to vertically and horizontally resolve spatial pat- melting (Yamamoto-Kawai et al., 2009; Wang et al., 2013). Likely terns of acidification during the seasonal onset, peak, and decline of due to a combination of these processes, some recent investigations hypoxia in these estuaries. Given the excessive productivity and of coastal zones have detected seasonally low pH and/or elevated organic matter loading within eutrophic estuaries, we hypothe- pCO2 conditions (Feely et al., 2010; Cai et al., 2011; Sunda and Cai, sized that pH and DO would co-vary and reach extremes lower than 2012; Duarte et al., 2013; Melzner et al., 2013), while others have those in the open ocean and most other coastal systems charac- documented that some coastal regions have experienced progres- terized to date. As a guide to possible impacts on ecosystem pro- sively declining pH levels in recent decades (Waldbusser et al., cesses, we evaluated the saturation state of the water column with 2011). respect to common biogenic carbonate minerals, specifically Ocean acidification has garnered much attention among scien- aragonite. tists, policy makers, and the public during the past decade. The term has generally been used to describe the ongoing decrease in 2. Methods surface ocean pH due to anthropogenic increases in atmospheric CO2 (Caldeira and Wickett, 2003). Since this acidification also de- This study characterized spatial and temporal patterns of DO, 2 U creases the availability of CO3 it can have negative consequences pH, pCO2, and aragonite in four, semi-enclosed estuarine systems for marine organisms, both pelagic and benthic, that produce across the Northeast US: Narragansett Bay (Rhode Island (RI), structures made of calcium carbonate (CaCO3; Ries et al., 2009; 41.63N, 71.37W), Long Island Sound (New York (NY)-Connecticut Talmage and Gobler, 2009; Gazeau et al., 2013) and has some- (CT), 41.11N, 72.86W), Jamaica Bay (NY, 40.61N, 73.84W), and times been deemed ‘The other CO2 problem’ (Doney et al., 2009). A Hempstead Bay (NY, 40.60N, 73.57W; Fig. 1). The Northeast US is similar perspective could be adopted with respect to eutrophica- the most heavily urbanized and populated region in the nation and tion processes, the literature on which generally emphasizes only contains some of the densest populations on the planet including nutrient-productivity-hypoxia relationships. Beyond calcifying or- the most populous US metropolis, New York City. Coastal waters in ganisms, information is mounting that acidification can also be this region have also been shown to have a lower buffer capacity damaging to some finfish (Munday et al., 2010), particularly during compared to the southeast and Gulf coasts of the US (Wang et al., early life stages (Baumann et al., 2012; Frommel et al., 2012; Murray 2013). We utilized three approaches for this study: 1) The anal- et al., 2014). While acidification in the open ocean is driven by ysis of monthly monitoring data across Long Island Sound; 2) external, atmospheric loading of CO2, in coastal zones this process Vertical measurements of water column conditions across Narra- may be minor compared to internal loading processes, particularly gansett Bay, Long Island Sound, and Jamaica Bay; and 3) Contin- within eutrophic regions where excessive nutrient loading and uous, horizontal mapping of conditions across Jamaica Bay and organic matter production have been associated with large hypoxic Hempstead Bay. All field work was performed during daylight. events. Long Island Sound (LIS; Fig. 1) is the third largest in the The goal of this study was to characterize the spatial and tem- US, and its western end receives more than four billion liters of poral dynamics of DO, pH, pCO2, and Uaragonite in the water columns treated wastewater effluent daily from the nation's largest of several representative, estuarine systems along the northern US metropolis, New York City. The combination of excessive waste- Atlantic coast (Fig. 1). Multi-year monitoring datasets were water loads and sluggish circulation have contributed toward the assessed to define seasonal patterns in pH and DO while cruises annual occurrence of hypoxia within western LIS since the middle

Fig. 1. Study sites. Long Island Sound CTDEEP sampling stations represented as black dots whereas small black dots surrounded by circles indicate CTDEEP sampling stations occupied for this study. Narragansett Bay in upper right box with black dots of inset indicating discrete sampling stations. Jamaica Bay and Hempstead Bay in small boxes at lower left, with black dots within inset depicting Jamaica Bay sampling stations. Upper left inset: Northeast US. R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 3 of the twentieth century (Parker and O'Reilly, 1991; O’Donnell et al., et al., 2014). The SeaFET pH sensor utilizes ion-selective field ef- 2014; Suter et al., 2014). The LIS Comprehensive Conservation and fect transistor (ISFET) technology coupled with a solid state refer- þ Management Plan was implemented in 1994 (USEPA, 1994), leading ence electrode to measure pH on the total H scale (pHT) and was to a nitrogen loading reduction target of 58%. This management calibrated annually by the manufacturer. A comparison of pHNBS plan further initiated monthly monitoring of LIS by the Connecticut and pHT scales demonstrated a typical offset of ~0.12 during this Department of Energy and Environmental Protection (CTDEEP). For study (pHT < pHNBS). Discrete water samples for the direct mea- this study, we compiled CTDEEP's measurements of DO and pHNBS surement of pHT and total dissolved inorganic carbon (DIC) were (pH on the National Bureau of Standards scale) from the start of its collected at multiple depths via Niskin bottles, preserved using a monitoring of both parameters in August 2010 through 2012. saturated mercuric chloride (HgCl2) solution, and stored at 4 C. DIC CTDEEP conducts vertical surveys at dozens of stations in LIS from measurements were made using an EGM-4 Environmental Gas ® New York City to the coastal Atlantic Ocean using a Sea-Bird Elec- Analyzer (PP Systems) after acidification and separation of the gas © ® tronics SBE 19 SEACAT CTD, transmitting data at 4 Hz. The SBE 19 phase from seawater using a Liqui-Cel Membrane (Membrana). was outfitted with a Seabird SBE 43 DO sensor (polarographic This instrument was calibrated using standards made from sodium membrane sensor); oxygen measurements were validated via bicarbonate and provided a methodological precision of ±0.85% for Winkler titration measurements (Parsons et al., 1984) of discrete replicated measurements. As a quality assurance measure, certified samples. The SBE 19 was also equipped with a Seabird 18 pH sensor reference material generated by Dr. Andrew Dickson's lab (Uni- equipped with a pressure balanced glass electrode/Ag/AgeCl versity of California San Diego, Scripps Institution of Oceanography; reference probe that provided pH measurements on the NBS scale. Batch 132 ¼ 2033 mmol DIC kg seawater 1) was analyzed in Prior to each survey, a three point calibration was conducted on the quadruplicate immediately before and after the analysis of every pH sensor using commercial buffer solutions (±0.02 pH). Finally, a set of samples and yielded full recovery (measured WET Labs WETStar fluorometer was used to measure in vivo values ¼ 104 ± 3.87% of certified values). Levels of pCO2 and Uar- chlorophyll a fluorescence which was converted to units of mg agonite were calculated based on pressure and measured levels of 1 chlorophyll a L using discrete measurements of extracted chlo- DIC, pHT, temperature, salinity, phosphate, silicate and first and rophyll a. For analyses presented here, measurements from the 17 second dissociation constants of carbonic acid in estuarine waters mid-estuarine stations that span the entire 150 km longitudinal according to Millero (2010) using the program CO2SYS (http://cdiac. extent of LIS were used to generate surface and bottom time series ornl.gov/ftp/co2sys/). The parameter Uaragonite is a measure of the plots (2010e2012) as well as vertical section plots using Ocean Data saturation state of the water with respect to aragonite and is 2þ 2 View (ODV 4.6.0; http://odv.awi.de/) over an annual cycle in 2011. defined as Uaragonite ¼ [Ca ][CO3 ]/Ksp,arag, where Ksp,arag is the 2þ 2 Following analysis of the CTDEEP data set, we performed cruises solubility product of Ca and CO3 . There are three common in 2012 and 2013 based on the hypothesis that the same processes biogenic carbonate mineral groups: aragonite, low-Mg calcite, and promoting hypoxia (intense microbial respiration) also acidify the high-Mg calcite, the latter having a spectrum of compositions and water column in coastal ecosystems. These cruises focused on the solubilites (Morse et al., 2007). We chose to use aragonite, a rela- western half of LIS that experiences hypoxia and has the strongest tively soluble mineral present in many invertebrate larval stages eutrophication gradient within this system (O'Shea and Brosnan, (Weiss et al., 2002), as a representative form. During this study, 2000; Gobler et al., 2006) and proceeded further towards New levels of pCO2 measured with the HydroC were nearly identical to, York City than cruises performed by CTDEEP. In 2012, cruises were and never significantly different, from levels calculated for discrete performed during mid- and late August when hypoxia has been samples based on DIC and pHT,afinding consistent with our prior historically most intense in LIS (Parker and O’Reilly, 1991; O’Shea use of this device (Baumann et al., 2014). Regressions of pCO2 levels and Bronsan, 2000; O'Donnell et al., 2014) whereas in 2013, five measured via the HydroC™ and those calculated from parallel cruises were performed between July and October to capture the discrete samples were highly significant (p < 0.001) with a corre- onset, peak, and demise of hypoxia. During each cruise, we lation coefficient exceeding 0.9 and a slope not significantly collected water samples from multiple depths using Niskin bottles different from 1.0. Discrete pHT measurements were also made on and vertically profiled the water column at eight stations across LIS vertically collected samples using a DuraFET III (Honeywell) ISFET- (Fig. 1) onboard the R/V Seawolf (Stony Brook University). Station based solid state pH sensor and were made spectrophotometrically locations were recorded using a GPS datalogger (Sparkfun elec- using m-cresol purple (Dickson et al., 2007). Measurements of pHT tronics, model: GeoChron Blue). A Sea-Bird Electronics SBE 9plus with the SeaFET were nearly identical to, and never significantly CTD, a Contros HydroC CO2 sensor, and a Satlantic SeaFET ocean pH different, from those obtained with the DuraFET III or spectro- sensor were affixed to a standard rosette sampler to provide photometric measurements; regressions of the various pH mea- continuous, vertical measurements of DO, temperature, salinity, surements were highly significant (p < 0.001) with correlation þ depth, pCO2, and pHT (pH on the total H scale). The SBE 9plus was coefficients exceeding 0.96 and slopes not significantly different equipped with a SBE 43 dissolved oxygen sensor described above, from 1.0. Vertical section plots of DO, pHT, pCO2 and Uaragonite in LIS transmitted at 24 Hz, was calibrated to 100% saturation in air prior were made using ODV 4.6.0. to use, and had an analytical precision of 2.1%. The HydroC and Narragansett Bay is the largest estuary in New England, USA, SeaFET sensors had analytical precisions of 1.4% and 0.09%, and is bordered by Rhode Island (RI) and Massachusetts (MA), as respectively, and transmitted at 1 and 0.3 Hz, respectively. The well as RI's largest city, Providence. Narragansett Bay is known to HydroC measures pCO2 concentrations via non-dispersive infrared experience regionally high levels of nutrient loading and hypoxia spectrometry (NDIR) after dissolved gasses within seawater (Nixon et al., 2008). To establish the levels of DO, pHT, pCO2, and permeate a hydrophobic membrane and equilibrate with the inner Uaragonite across Narragansett Bay during summer, monthly cruises pumped gas circuit (Fiedler et al., 2012; Fietzek et al., 2014). A were performed from June through August of 2013. The water laminar flow pump (Sea-Bird Electronics) affixed to the HydroC column was vertically sampled at seven geo-referenced stations continuously delivers seawater across the sensor membrane. The across the complete latitudinal gradient of the estuary from the HydroC was calibrated annually using sodium carbonate and bi- brackish regions of the Seekonk River to the region where the Bay carbonate standards (200, 400, 800, 1600, 2400, 3200, 4000 matm) exchanges with Block Island Sound (Fig. 1). Cruises were conducted in quantities mimicking the CO2 buffer system of seawater (DIC:TA) onboard the USEPA's R/V Coastal Explorer from which Niskin bottles, and ran internal blanks every five minutes while in use (Fietzek the HydroC CO2 sensor, and a YSI 6920 V2-2 (Yellow Springs, Inc) 4 R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 sonde were used to vertically assess levels of pCO2, temperature, salinity, and DO concentrations. The 6920 V2 was equipped with a ® YSI 6560 conductivity/temperature probe, and a YSI 6450 ROX optical DO sensor with an analytical precision of 4%. Each probe was separately calibrated prior to deployments using a 50,000 mScm 1 conductivity solution and air saturated distilled water, respectively. Discrete water samples were collected at multiple depths at each station using Niskin bottles and preserved to make discrete mea- surements of DIC and pHT as described above. Chlorophyll a in discrete samples was quantified according to Parsons et al. (1984). Vertical section plots of DO, pHT, pCO2 and Uaragonite were made as described above. Jamaica Bay is a hypereutrophic lagoonal estuary located within the New York City boroughs of Brooklyn and Queens, and receives ~90% of its nitrogen load from four major wastewater-treatment plants that discharge ~ one billion liters of treated effluent daily (Benotti et al., 2007). Vertical sampling of Jamaica Bay was per- formed at five stations across northeastern Jamaica Bay (Fig. 1) during the peak (August) and decline (September, November) of hypoxia. Vertical profiles of DO, pHT, and pCO2 were generated using the HydroC CO2 sensor, the SeaFET pH sensor, and the YSI 6920 V2-2 sonde as described above. Vertical section plots of DO, pHT, pCO2 and Uaragonite were made as described above. Levels of DO and pCO2 were profiled horizontally across Hempstead Bay and Jamaica Bay, NY, US, during the fall of 2011. Hempstead Bay is a eutrophic lagoon comprised of intermittent salt marshes and dredged navigational channels. The Bay Park sewage treatment plant receives wastewater from more than a half million homes in Nassau County, NY, and discharges 200 million liters of treated effluent per day into Hempstead Bay. Both horizontal mapping cruises were performed using the HydroC CO2 sensor and YSI 6920 V2-2 sonde affixed 0.5 m below the water surface to a bracket on a small vessel that proceeded ~1 m s 1 to minimize turbulent mixing around sensors. Cruise tracks were geo- Fig. 2. Time series of DO and pHNBS, August, 2010eOctober, 2012. A) Western Long referenced using a GPS datalogger (Sparkfun electronics, Geo- Island Sound, bottom & B) surface. C) Eastern Long Island Sound, bottom & D) surface. Chron Blue). The cruise through Hempstead Bay began at the Jones Inlet to the Atlantic Ocean, progressed past the Bay Park sewage treatment plant outfall, and north into Hempstead Bay. In Jamaica While oxygen and pH levels were normal throughout the water 1 Bay, the cruise began within the northeastern extent of the Bay column in LIS during May (pHNBS > 8; DO > 7.5 mg L ; Fig. 3), these receiving >300 million liters per day of treated wastewater effluent, conditions changed with the onset of summer. Specifically, pH and ended within the inlet to the Atlantic Ocean. Maps of contin- levels were lower throughout LIS in June, while DO levels began to ually measured levels of DO and pCO2 were generated using ArcGIS decline in western bottom waters (Fig. 3). During July, August, and 10 (ESRI, Redlands, CA). September, hypoxic and acidified conditions were present in 1 western LIS as DO levels declined to <3mgL and pHNBS levels 3. Results decreased to <7.4 (Fig. 3). These conditions developed despite a continuous layer of dense algal biomass (chlorophyll a >30 mgL 1) Over an annual cycle, levels of pHNBS and DO were strongly in surface waters of western LIS (Fig. 3). In October, higher levels of coupled and highly dynamic within the western extent of LIS, DO and lower levels of algal biomass were present throughout LIS, particularly within bottom waters where peak levels of pHNBS (8.76) but low pH (7.7) persisted in western LIS (Fig. 3). By November, pH and DO (11.83 mg L 1) occurred in winter coincident with the and DO levels throughout the entire water column were similar to winterespring bloom and minimal values of 7.23 and 0.94 mg L 1, May being >7.9 and >7.5 mg L 1, respectively (Fig. 3). respectively, occurred during summer (Fig. 2A). Similar temporal Given the co-occurrence of hypoxia and acidification in western patterns occurred within surface waters of western LIS, although LIS during August of 2010 and 2011, a cruise focusing on the the values were less extreme with pHNBS ranging from 8.32 in western half of LIS was performed to assess the levels of pCO2 and 1 winter to 7.48 in summer and DO ranging from 13.1 mg L in Uaragonite present in August 2012. While the surface mixed layer of 1 1 winter to 5.33 mg L during summer (Fig. 2B). Within eastern LIS, eastern LIS had elevated levels of pHT and DO (>7.7, >7mgL ), similar temporal patterns were observed for DO, although the moderate pCO2 levels (~500 matm), and was saturated with respect 1 range in values was smaller for bottom (4.86e11.5 mg L ; Fig. 2C) to aragonite (Uaragonite > 1; Fig. 4), these conditions deteriorated and surface waters (6.43e11.7 mg L 1; Fig. 2D) compared to significantly to the west, particularly within bottom waters. Spe- western LIS. pHNBS within eastern LIS also had a smaller dynamic cifically, nearly all bottom waters of LIS had pHT values <7.5, DO 1 range (7.43e8.57), was similar between surface and bottom waters, concentrations <4mgL , pCO2 concentrations >1500 matm, and and displayed a less distinct seasonal pattern. were undersaturated with respect to aragonite (Uaragonite < 1; A cross sectional examination of chlorophyll a, pH and DO in LIS Fig. 4). The most extreme of these conditions were found in the far revealed the vertical, horizontal, and temporal evolution of west where bottom DO values were <2mgL 1 (Fig. 4), and pH phytoplankton biomass, hypoxia, and acidification in this system. levels were low throughout the water column and in some cases R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 5

Fig. 3. Monthly vertical section plots of DO (measured via a SBE 43 DO sensor), pHNBS (measured via a Seabird 18 pH sensor), and chlorophyll a (Chl-a; measured via a WET Labs WETStar fluorometer) with temperature in C (measured via a SBE 19 SEACAT CTD) contour lines during MayeNovember 2011 in Long Island Sound. Vertical lines indicate CTD profiles. Depth is 0e45 m.

were acidic (<7.0; Fig. 4). Concentrations of pCO2 in the west were acidification and high pCO2 throughout the water column, whereas extremely high (>2500 matm) in both surface and bottom waters these conditions were confined to bottom waters and were less and Uaragonite was <0.5 throughout the entire water column in intense to the east (Fig. 5). While surface waters of LIS were satu- western LIS (Fig. 4). A second cruise in LIS during late August of rated with respect to aragonite during July, nearly all of LIS was 2012 showed the spatial distribution and levels of pCO2 and pHT undersaturated during early August (Uaragonite < 1; Fig. 5). Pro- were highly similar to the first cruise, while levels of DO were gressing into the fall, Uaragonite gradually improved in most of LIS slightly higher (>2mgL 1; data not shown). (Fig. 5). While LIS was well oxygenated by October of 2013 In 2013, cruises were performed July through October in LIS to (>7mgL 1), bottom waters in the far west retained clear signs of better assess the temporal dynamics of carbonate chemistry in acidification (pH < 7.7; pCO2 > 1000 matm; Uaragonite < 1; Fig. 5). conjunction with hypoxia and acidification. While the spatial dy- Like many river fed estuaries, Narragansett Bay exhibits a namics of DO, pH, pCO2 and Uaragonite in 2013 were similar to 2012, stronger vertical salinity gradient than LIS, particularly within its the intensity of hypoxia was lower, as bottom DO levels remained northern extent. Regardless, the two systems displayed similar 1 above 2.4 mg L during all sampling (Fig. 5). Despite the lesser horizontal and vertical gradients of DO, pH, pCO2, and Uaragonite intensity of hypoxia, low pH (<7.2) and high pCO2 (>2500 matm) during summer months. For example, in June much of the water conditions again developed during August of 2013 (Fig. 5). In a column within the northern, lower salinity region of the Bay had 1 manner similar to 2012, the western-most region experienced low DO (<4mgL ), low pHT (<7.5) and high pCO2 (>1000 matm), 6 R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13

fully oxygenated by November following Hurricane Sandy, the system retained slightly reduced pHT (<7.9) and mildly elevated pCO2 levels (>700 matm; Fig. 7). Horizontal mapping of surface waters within lagoons receiving large volumes of wastewater discharge further linked DO and pCO2 levels in estuarine waters. For example, during a cruise across Ja- maica Bay that began within its northeastern extent and ended within the Atlantic Ocean inlet, levels of pCO2 steadily decreased from >4000 matme~500 matm, while DO levels increased in parallel from <2mgL 1 to 7 mg L 1 (Fig. 8A and B). There were strong correlations between concentrations of pCO2 and salinity 2 2 (r ¼ 0.92; Fig. 8C) as well as between pCO2 and DO (r ¼ 0.95; Fig. 8D). Finally, mapping of Hempstead Bay surface waters further demonstrated the strong influence sewage treatment plant outfalls have on pCO2 levels within an estuary. While nearly all of Hemp- stead Bay, from the Atlantic Ocean through the northern extent of the system, had levels of pCO2 that ranged from 450 to 700 matm, the 3 km of the cruise track to both the east and west of the Bay Park sewage treatment plant outfall pipe had higher pCO2 levels that ranged from 700 to 1200 matm (Fig. 9). There was not a rela- tionship between pCO2 and salinity in this system. Because all of these measurements were made during daylight and thus periods of photosynthetic activity, they likely represent minimum esti- mates of surface water pCO2.

4. Discussion

This study revealed that acidification is an annual feature of eutrophic estuaries across the Northeast US that co-occurs with seasonally low oxygen. The spatial and temporal dynamics of DO, pH, pCO2, and Uaragonite suggest that they are all ultimately driven by the same processes, namely high rates of microbial respiration fueled by nutrient enriched algal organic matter coupled with water column stratification. The degree of acidification observed in these systems during summer are within ranges that have been shown to adversely impact a wide range of marine life (Ries et al.,

Fig. 4. Vertical section plots of DO (measured via a SBE 43 DO sensor), pHT (measured 2009; Kroeker et al., 2010; Harvey et al., 2013; Kroeker et al., U via a SeaFET pH sensor), pCO2 (measured via a HydroC CO2 sensor), and aragonite (both 2013). As such, this study provides new insight regarding the calculated from discrete measurements of DIC and pH via a Durafet III sensor) with extent of coastal acidification as well as evidence that it represents temperature in C (measured via a SBE 9plus CTD) contour lines during August of 2012 a significant, but previously underappreciated environmental in Long Island Sound. Vertical lines indicate CTD profiles. Depth is 0e40 m. threat. resulting in water that was undersaturated with respect to arago- 4.1. The co-evolution of hypoxia and acidification in estuaries nite (Uaragonite < 1; Fig. 6). While oxygen levels within the southern extent of the Bay were high through nearly all of the water column The acidification of coastal systems is a seasonal phenomenon in June (>7mgL 1), bottom waters across the entire bay displayed that displays a high degree of temporal and spatial coherence signs of acidification with pHT < 7.7, pCO2 >1000 matm, and Uar- with DO levels (Cai et al., 2011; Sunda and Cai, 2012; Melzner agonite < 1.5 (Fig. 6). During July and August, this acidification et al., 2013; this study). It has been well established that eutro- pattern persisted in Narragansett Bay with values of pHT, pCO2, and phic coastal zones that receive large amounts of organic matter Uaragonite being similar to June, whereas DO levels across the loading are vulnerable to hypoxia during warmer months as rapid southern extent of Bay declined in July (<7mgL 1), and again in microbial respiration rates consume oxygen faster than it is August (<6mgL 1; Fig. 6). replenished by horizontal or vertical ventilation (Rabalais et al., Jamaica Bay is a lagoonal estuary that historically experiences 2002). The northeast US has been shown to host some of the hypoxia during summer months within its northern and eastern largest nutrient loading rates in the world that promote organic channels. During August of 2012, vertical and horizontal mea- matter production by primary producers as well as rapid rates of surements within these regions revealed that, in addition to being respiration by heterotrophs (Anderson and Taylor, 2001; Howarth, hypoxic (<3mgL 1), much of the water column within Jamaica Bay 2008). Along with oxygen consumption microbes release meta- was acidified (pHT < 7.4) and had levels of pCO2 exceeding bolic CO2, which in turn reacts with the seawater carbonate sys- 2000 matm with bottom waters displaying extremes in these con- tem causing acidification or a lowering of seawater pH. All 1 ditions (DO < 2mgL ,pHT < 7.2, pCO2 > 3000 matm; Fig. 7). In systems presented here had pCO2 > 1000 matm during summer September, much of water column re-oxygenated to >7mgL 1 months, while regions exposed to extreme eutrophication (e.g. with the exception of eastern bottom waters (<6mgL 1; Fig. 7). >billion liters sewage effluent per day; LIS, Jamaica Bay) experi- The water column was slower to recover from acidification, how- enced >3000 matm pCO2 and acidic seawater (pH < 7.0). Summer ever, as September pCO2 levels ranged from 700 to 1300 matm while changes in temperature account for <5% of these pCO2 increases. pHT levels were generally <7.7 (Fig. 7). While the water column was Such pCO2 conditions are not expected to occur in the open ocean R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 7

Fig. 5. 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 temperature (C, measured via a YSI 6920 V2) contour lines during July, early August, late August, September, and October of 2013 in Long Island Sound. Vertical lines represent CTD profiles. Depth is 0e40 m. within the next hundred years, if ever, given projected anthro- exhibited the lowest pH and DO levels during summer. pogenic CO2 increases from fossil fuel emissions (I.P.C.C. 2007). Conversely, the eastern portions of this system have lower We hypothesize that the present acidification of coastal systems is nutrient levels (Supplementary Fig. 1) and algal biomass (Fig. 3) a function of the intensity of nutrient loading rates. The links and retained higher pH and DO levels through the year, even in 1 between acidification, hypoxia, and eutrophication were well- bottom waters (pHNBS > 7.7; DO > 5mgL ). Similarly, within illustrated within LIS where regions near New York City Narragansett Bay and Jamaica Bay, the regions of the estuaries receiving the heaviest loads of nutrients, experiencing the highest with the most intense algal blooms and highest nutrient con- nutrient levels (Supplementary Fig. 1), and hosting the most centrations (Supplementary Figs. 2 and 3) were the same regions intense algal blooms (this study; Gobler et al., 2006)also 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. 8 R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13

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 detected in all four study sites, particularly in bottom waters. with enhanced nutrient loading that stimulates phytoplankton Furthermore, in stratified, deeper systems (LIS, Narragansett Bay), blooms (Nixon 1995) and, via photosynthesis, should consume CO2 there can be a spatial decoupling of productivity, hypoxia, and and increase pH levels. Indeed, our analysis of annual pH cycles in acidification with high productivity confined to surface layers, and LIS demonstrated that the winterespring phytoplankton bloom low DO and pH found extensively across bottom waters. In other period was associated with highly basic pH values (>8.5; Fig. 2). cases, however, strong summer hypoxia and acidification existed in These peak pH values, usually during February in LIS and other the presence of elevated levels of algal biomass (e.g. Fig. 3, western systems (Baumann et al., 2014), are followed by a progressive LIS in September 2011; Fig. 7, Jamaica Bay in August 2012). decline in pH by more than one unit to < 7.5 during summer and fall While comprehensive surveys of pH and pCO2 within estuaries as microbial respiration rates intensify. Therefore, while eutrophi- are not common, some preliminary hypotheses can be developed cation does promote algal blooms that can raise the pH and DO of regarding the types of systems that may be the most prone to surface waters in winter, the remineralization of this algal organic acidification based on this and prior studies. Measurements of matter during summer and fall leads to the seasonal acidification 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. R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 9

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 upwelling- induced 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 sur- veys 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 Fig. 9. Surface pCO2 levels in Hempstead Bay as measured via a HydroC CO2 sensor had substantially lower pH and buffering capacity than all other 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. 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 93% were net heterotrophic, experiencing an annual net con- present study. sumption of DO (Caffrey, 2004) and thus production of pCO2 and While hypoxia and acidification co-occurred in estuaries during likely some degree of seasonal acidification. Among the 20 salt summer, some observations suggest low pH conditions may persist marsh-dominated estuaries surveyed by Caffrey (2004), all were longer into the fall than low oxygen. For example, during 2011 and net heterotrophic. Salt marshes host extreme levels of microbial 2013 in LIS and during 2012 in Jamaica Bay, waters transitioned metabolism (Dame et al., 1986; Koch and Gobler, 2009) and the two from hypoxic to normoxic during early fall (October) but main- lagoons studied here (Jamaica and Hempstead Bay) have significant tained pHT levels < 7.7. These differences may be a function of the stands of salt marsh. As such, beyond eutrophication-driven acid- differential diffusion and solubility of O2 and CO2 as a function of ification, salt marshes may have also promoted the high pCO2 temperature (Millero et al., 2006). Cooler fall temperatures enhance conditions in these shallow systems. Our recent 5-yr study of gas solubility, and may contribute toward a more extended period another NY salt marsh (Flax Pond) found a highly significant cor- of acidification during fall compared to hypoxia, even in the face of relation between DO and pH and extreme acidification in summer, slowing microbial respiration. In the case of DO, cooler tempera- particularly during low tides and at night (pCO2 >4000 matm; tures will lead to a diffusion of oxygen into water whereas in the Baumann et al., 2014). case of CO2, cooler temperatures will slow the diffusion out of Conversely, high rates of autotrophy make seagrass meadows a water. An additional factor that likely enhances acid production significant sink for carbon (Duarte et al., 2010). Accordingly, (lower pH) during times when DO levels are increasing is the seagrass-dominated estuaries, which must be shallow to host such oxidation of anaerobic metabolites. The reduced constituents (e.g., þ 2þ 2þ benthic vegetation, are often net autotrophic (Caffrey, 2004) and NH4 ,HS ,Fe ,Mn ) that build up in surface sediments during are likely to buffer against ocean acidification in the water column hypoxia oxidize seasonally when systems re-oxygenate (Soetaert (Hendriks et al., 2014). Beyond the photosynthetic activity of the et al., 2007). These oxidation reactions produce strong acids that submerged aquatic vegetation, shallow estuaries are also more titrate alkalinity, lower pH, and could promote shell dissolution in likely to be well-mixed, rapidly equilibrating with atmospheric CO2, bivalves (Green and Aller 1998). As such, the seasonal duration of and thus may be generally less vulnerable to continued respiratory acidification as a selective pressure in estuarine organisms may be acidification than deeper systems (such as LIS) that are typically longer than the seasonal pressures imposed by hypoxia. stratified in summer and have a smaller fraction of the water col- Beyond microbial respiration driven by internal, autochtonous umn within the euphotic zone. These shallow systems may, how- sources of organic carbon, this study provides evidence that the ever, be vulnerable to large diurnal variations in pH and DO discharge of wastewater from sewage treatment plants is a previ- particularly in cases of excessive loadings of organic matter ously unappreciated, point source of acidification and high pCO2 (Baumann et al., 2014). Shallow estuaries are more responsive to water in coastal zones. While these low pH conditions may be nutrient loading and often shift from net autotrophic to net het- partly a function of microbial respiration of the allochthonous erotrophic on diel timescales with the intensity of these shifts organic matter discharged from sewage within the estuary, it is also linked to the intensity of nutrient loading (O'Boyle et al., 2013). likely the discharged sewage itself is acidified. This was most Given that all of the surveys presented here occurred during the obvious during our horizontal cruises across the lagoons in south- day, the extent of acidification in some of these systems is likely west Long Island where a radius of several kilometers of estuarine even more extreme at night, particularly within shallow regions. surface waters around sewage outfall sites had levels of pCO2 near Finally, extended residence times within estuaries are likely to or above 1000 matm (several times supersaturated). The surface exacerbate acidification as poorly flushed waters will be more likely waters of western LIS are highly enriched in wastewater (Sweeney to accumulate pCO2 during periods of intense organic matter and Sanudo-Wilhelmy, 2004) and had surface waters with nearly remineralization. the same low pH and high pCO2 as bottom waters during summer Coastal acidification in the US has been most commonly and fall. Due to its high organic matter load, wastewater experi- examined along the Pacific coast where deep, pCO2-enriched wa- ences extreme amounts of microbial respiration and has been ters are seasonally upwelled (Feely et al., 2008, 2010; Hofmann previously shown to be low in pH (6e8) and DO (at times anoxic) et al., 2011) and negatively impact oyster populations in and enriched in pCO2 (Gallert and Winter, 2005). A management 10 R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 goal for LIS (USEPA, 1994) and other coastal systems is to remove N system: While its western extreme receives large nutrient inputs from wastewater to relieve the symptoms of eutrophication from NYC (Parker and O’Reilly, 1991; O’Shea and Bronsan, 2000) including hypoxia (Nixon and Buckley, 2002). Given that the and can be acidic (pH < 7), the eastern end exchanges with the removal of N is generally achieved via increased microbial activity Atlantic Ocean and is fairly oligotrophic (Gobler et al., 2006). (i.e. biological denitrification), this enhanced level of N removal may yield effluent with lower pH and high pCO2 levels (Soetaert 4.2. Biological implications et al., 2007). As such, it is possible that coastal regions in close proximity to wastewater discharge may experience more intense This study establishes that estuarine pelagic organisms in acidification as treatment plants are upgraded with higher amounts temperate zones are commonly exposed to acidification and waters of denitrification to alleviate other symptoms of eutrophication. undersaturated with regard to aragonite during summer and fall Given the chronically high concentrations of pCO2 in regions within months. Consistent with our study, Feely et al. (2010) reported that close proximity to sewage treatment plant discharge (>1000 matm), most of Puget Sound, WA, USA, was undersaturated with regard to it seems likely that these sites may have a localized impact on the aragonite during August. The summer levels of pH, pCO2, and surrounding flora and fauna in a manner that parallels other calculated Uaragonite present through large areas within the estu- concentrated sources of pCO2 including volcanic seeps (Fabricius aries studied here during summer (pH < 7.7T, pCO2 > 1000 matm, et al., 2011). Uaragonite < 1) are within the range that have been shown in labo- The connection between eutrophication and acidification was ratory studies to reduce the growth and survival of early life stage further evidenced by the relationship between DO and pH for the mollusks (Gazeau et al., 2013) and fish (Baumann et al., 2012; three major systems studied here: LIS, Narragansett Bay, and Ja- Frommel et al., 2012; Chambers et al., 2013). Furthermore, these maica Bay (Fig. 10). For all of the sites, there was a highly significant, conditions emerge at the same times that many mollusks and fish linear relationship between DO and pH (p < 0.0001), with Jamaica spawn in estuaries (Kennedy and Krantz, 1982; Bricelj et al., 1987; Bay displaying the strongest relationship (R ¼ 0.94) and LIS Able and Fahay, 1998; Kraeuter and Castagna, 2001), suggesting showing more variance (R ¼ 0.70). The correlation for Jamaica Bay that some early life stage fish and mollusks sensitive to acidification was slightly improved with a logarithmic fit(R ¼ 0.94). This vari- may be negatively impacted by high levels of pCO2 and low levels of ability in LIS was partly a function of the depth of this system as pH and carbonate. Therefore, we suggest that acidification should during summer, stratified conditions, DO levels were largely uni- be considered among the factors that shape fisheries yields in form below the mixed layer, while pH levels continued to decline to coastal zones. A vivid example of this may be the bay scallop the bottom. General linear regression models of the DO-pH rela- (Argopecten irradians) which is known to spawn in mid-to-late tionship for each system provided y-intercept values for Jamaica summer (July, August) and is one of the organisms most sensitive Bay, LIS, and Narragansett Bay of 7.07, 7.14, and 7.25, respectively, to acidification (Talmage and Gobler, 2009, 2010, 2011), experi- representing the levels of pHT predicted under anoxic conditions encing significant declines in survival when exposed to (DO ¼ 0; Fig. 10). These values further emphasize linkages between pCO2 750 matm for only four days (Gobler and Talmage, 2013). eutrophication and acidification. Jamaica Bay receives ~90% of its N While the collapse of this fishery in NY waters was caused by toxic load from sewage discharge (Benotti et al., 2007) and is predicted to algae blooms decades ago (Gobler et al., 2005), the failure of this experience the most extreme acidification under anoxic conditions population to recover despite significant restoration efforts may be (pHT ¼ 7.07). In contrast, Narragansett Bay experiences excessive caused, at least in part, by the overlap of annual spawning events nutrient loading within its northern extent, but is a more oligo- with acidified conditions in estuaries. We note that during this and trophic system to the south (Nixon et al., 2008), and was predicted prior studies (Baumann et al., 2014), there has been significant to experience the highest pHT under anoxic conditions (7.25). LIS interannual variation in the intensity and timing of acidification was similar to Jamaica Bay (anoxic pHT ¼ 7.14), but was not as with warmer spring and summers being associated with earlier extreme, again likely reflecting the more hybrid nature of this 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 func- tion of differences between exposure levels for benthic and pelagic organisms as well as the differential susceptibility and de- mographic 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 acidifica- Fig. 10. All paired measurements (n ¼ 6652) of surface pH and DO from LIS, Jamaica T tion near or in the benthos (Green et al., 1998), in highly eutrophic 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, systems during summer (e.g. western LIS and Jamaica Bay), the 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. entire water column was undersaturated with regard to aragonite, R.B. Wallace et al. / Estuarine, Coastal and Shelf Science 148 (2014) 1e13 11 suggesting even pelagic species and life stages will be exposed to regions prone to hypoxia should consider the concurrent effects of conditions unfavorable for calcification. acidification on these animals. Further, nutrient management plans We commonly observed pCO2 > 1000 matm in bottom waters in acidified estuaries may consider the level of nutrient load during summer months, with the most eutrophic estuarine regions reduction required to alleviate low pH conditions and the associ- exhibiting >3000 matm pCO2 and acidic seawater (pH < 7.0). These ated impacts on marine life. Finally, given that rising atmospheric observations demonstrate that the recommendation to restrict CO2 levels will further depress estuarine pH levels (Miller et al., ocean acidification experiments with marine organisms to pCO2 2009), the importance of management efforts that address levels of 1000 matm and below to mimic future climate change coastal acidification will continue to increase through this century. (Riebesell et al., 2010) should be heeded for open ocean species only. Indeed, given that estuarine organisms persisting within Acknowledgments deeper regions of the systems studied here may rarely experience pCO2 below 1000 matm during summer months, experiments This research was supported by NOAA's Ocean Acidification designed to assess the realistic effects of current and future acidi- Program through award #NA12NOS4780148 from the National fication on coastal species will need to target pCO2 levels signifi- Centers for Coastal Ocean Science, the National Science Foundation cantly beyond 1000 matm. (NSF # 1129622), and the Chicago Community Trust. In addition to acidification, this study further demonstrates the well-known tenet that estuarine organisms are often challenged by Appendix A. Supplementary data the stress of hypoxia during summer (Rabalais et al., 2002; Diaz and Rosenberg, 2008). Furthermore, in some cases, estuarine organisms Supplementary data related to this article can be found at http:// already existing near their upper temperature threshold may dx.doi.org/10.1016/j.ecss.2014.05.027. experience concurrent thermal stress (Portner€ 2008, 2010). Hence, it would seem the ‘hot, sour, and breathless’ (high temperature, low References pH, low DO) conditions predicted for the future open ocean (Gruber et al., 2011) can already be found in today's coastal zones during Able, K.W., Fahay, M.P., 1998. The First Year in the Life of Estuarine Fishes in the summer, and especially within the benthos where pH and DO levels Middle Atlantic Bight. Rutgers University Press. Anderson, T.H., Taylor, G.T., 2001. Nutrient pulses, blooms, and seasonal are generally lower than the water column (Zhu et al., 2006). Prior hypoxia in western Long Island Sound. 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