The combined effects of acidification and hypoxia on pH and aragonite saturation in the coastal waters of the California current ecosystem and the northern Gulf of Mexico
Introduction
The decrease in pH and aragonite saturation state, coupled with the increase in partial pressure of CO2 (pCO2), of subsurface coastal waters over time from the combined effects of acidification and respiration processes represents a developing and, in some cases, present-day threat to calcifying and non-calcifying marine organisms across the range of different life stages, taxa and habitats (Barton et al., 2012, Barton et al., 2015, Bednaršek et al., 2016, Doney et al., 2009a, Doney et al., 2009b, Doney, 2010, Fabry et al., 2008, Feely et al., 2004, Feely et al., 2008, Feely et al., 2016, Frieder et al., 2014, Gattuso and Hansson, 2011, Gattuso et al., 2015a, Gruber et al., 2012, Guinotte and Fabry, 2008, Hauri et al., 2013, Hettinger et al., 2012, Hofmann and Todgham, 2010, Kroeker et al., 2013, Lischka et al., 2011, Mackas and Galbraith, 2012, Manno et al., 2012, Orr et al., 2005, Somero et al., 2016, Waldbusser et al., 2015, Weisberg et al., 2016). Acidification of surface waters, resulting from the oceanic uptake of approximately 28% of the global anthropogenic carbon dioxide emissions has caused a lowering of average surface water pH by about 0.11 units and 0.5 units in aragonite saturation state (Feely et al., 2004, Feely et al., 2009, Feely et al., 2012, Gattuso et al., 2015a). Oxidative breakdown of organic matter sinking through the water column in subsurface waters can further reduce the pH and aragonite and calcite saturation state via respiration processes which are often enhanced in highly productive estuarine and coastal waters (Fig. 1c). How these processes interact and are impacted by changing temperature, salinity, gas solubility, and carbonate chemistry has been explored for pH and calcite saturation state for the Gulf of Mexico, East China Sea, and Baltic Sea (Cai et al., 2011, Sunda and Cai, 2012, Laurent et al., 2017).
Increased acidification and hypoxia are related because aerobic respiration of organic matter consumes oxygen and produces CO2 in approximate stoichiometric equivalence (Redfield et al., 1963):(CH2O)106(NH3)16H3PO4 + 138O2 ⇄ 106CO2 + 16HNO3 + H3PO4 + 122H2O
Thus, processes that create subsurface oxygen deficits can also exacerbate acidifying conditions for marine organisms. Here we build upon earlier work and compare the results of our recent studies of the chemical composition of surface and subsurface waters from the coastal waters of the California Current Ecosystem with previously published data from the Gulf Mexico to show how significant differences in gas solubility, Revelle factor, and temperature affect in-situ chemical conditions in the water column of a cold-water upwelling coastal environment.
As atmospheric CO2 increases and equilibrates with seawater, hydrogen ion (H+) and bicarbonate (HCO3–) is produced and carbonate ion (CO32-) is consumed via a series of chemical reactions:CO2(atmos) + H2O ⇄ CO2 (aq) + H2CO3;whereK0* = ([CO2(aq)]+[H2CO3])/pCO2H2CO3 ⇄ H+ + HCO3–;whereK1* = [H+][HCO3–]/([CO2(aq)] + [H2CO3])HCO3- ⇄ H+ + CO32–;whereK2* = [H+][CO32–]/[HCO3-]Ca2+ + CO32– ⇄ CaCO3s;whereKsp* = [Ca2+][CO32-]·
The air-sea CO2 exchange reaction (2) leads to an initial increase in dissolved CO2 in surface waters from gas exchange. The dissolved CO2 reacts with H2O to form carbonic acid (2). A portion of the carbonic acid quickly dissociates into a hydrogen ion and a bicarbonate ion (3), with K1* being the dissociation constant for (3). The bicarbonate ion can dissociate into a hydrogen ion and a carbonate ion (4), and K2* is the dissociation constant for (4). In addition, dissolved calcium (Ca2+) can combine with CO32- to form a calcium carbonate (CaCO3) mineral such as aragonite or calcite (5), with Ksp* being the stoichiometric solubility product at saturation for calcium carbonate. The net result is that the addition of CO2 from the atmosphere leads to overall increases in hydrogen ion and bicarbonate and decreases in carbonate ion as is illustrated below in a combined equation:CO2(aq) + H2O + CO32– ⇄ 2HCO3- and Knet = K1*/K2* = [HCO3-]2/([CO2(aq)] × [CO32–])
Another important factor related to the carbonate chemistry is the efficiency with which the oceans can continue to absorb more CO2 from the atmosphere and convert it to dissolved inorganic carbon (DIC), which is the sum of all carbonate species concentrations in µmol kg−1. This efficiency is defined as the Revelle Factor (RF):where pCO2 is the CO2 partial pressure in µatm. In ocean surface waters, the RF generally ranges from 8 to 18, with the lower values in warm subtropical waters and the higher values in the cold high-latitude regions (Sabine et al., 2004, Sabine and Tanhua, 2010, Egleston et al., 2010). Note that higher RF indicates lower buffering capacity.
As the oceans take up more anthropogenic CO2, the RF increases indicating that both the pCO2 increase and pHT (pH expressed in the total hydrogen ion concentration scale) decrease will be larger for each 1 µmol kg−1 increase in DIC. Consequently, we might also expect to see more extensive changes and higher seasonal variability of these parameters in colder less buffered waters.
In the late summer of 2013, we studied the extent of acidified conditions along the West Coast of North America from the coastal region off Washington, Oregon, and northern California. We conducted detailed chemical and hydrographic measurements in the region in order to better understand the relationships among these natural and human-induced processes that lead to acidification of the water column and their impact on pHT and aragonite saturation. Some parts of the California Current Ecosystem are particularly vulnerable because of the combined effects of acidification, warming, upwelling, and hypoxia, which are enhanced in the late summer and early fall months when respiration-induced oxygen depletions are at their maximum extent (Booth et al., 2012, Chan et al., 2008, Chan et al., 2017, Feely et al., 2008, Feely et al., 2016, Grantham et al., 2004, Hales et al., 2006, Harris et al., 2013, Hickey, 1979, Rykaczewski and Dunne, 2010, Siedlecki et al., 2016, Thomson and Krassovski, 2010, Turi et al., 2016). Ocean acidification (OA) decreases the concentration of CO32-, presenting a challenge for many marine calcifiers (Eq. (5)). One measure of the thermodynamic favorability for the precipitation of CaCO3 is saturation state. The saturation states of aragonite (Ωar) and calcite (Ωcal) are a function of the concentrations of dissolved Ca2+ and CO32-, and the temperature and pressure‐dependent stoichiometric solubility product,Ωar = [Ca2+][CO32-]/Kspar*Ωcal = [Ca2+][CO32-]/Kspcal*
such that Ωar and Ωcal will decline as more CO2 is taken up by the oceans. At Ω = 1, the carbonate minerals are in equilibrium with the surrounding seawater; at Ω > 1, precipitation or preservation of carbonate minerals is thermodynamically favored; and at Ω < 1, dissolution is favored (Mucci, 1983). The stoichiometric solubility products, Kspar* and Kspcal*, increase with increasing pressure and decreasing temperature such that as temperature decreases and/or pressure increases Ωar and Ωcal decrease.
Although Ω=1 is commonly referenced as an abiotic threshold for CaCO3 dissolution and precipitation, it is important to note that biogenic shell processes are not tightly bound to the Ω = 1 threshold. Instead, decreases in dissolution and calcification occur at various Ω values. For example, depending on the organismal life stage, shell dissolution in various marine calcifiers can start at Ω values ranging from 1.3 to 1.6 (Bednaršek et al., 2014; Waldbusser et al., 2015), while shell calcification can also occur at Ω values < 1 (Comeau et al., 2010), although at much reduced level (Langdon and Atkinson, 2005, Bednaršek et al., 2017). With decreasing Ω, organisms have to compensate against energetically more expensive processes and maintenance costs (O’Donnell et al., 2013, Wood et al., 2008).
While Ω predominantly affects marine calcifiers, pCO2 as a stressor can negatively affect both calcifiers and non-calcifers, subjecting them to the stress of hypercapnia. Hypercapnia is associated with the exposures of 1000 uatm pCO2 for more than one month (McNeil and Sasse, 2016). Elevated pCO2 and the attendant increased H+concentrations in the extracellular space lead to changes in the acid-base balance and organismal internal acidosis. Hypercapnia exposure in lower marine invertebrates with poor capacity to compensate for pH change results in metabolic depression, reduced level of protein synthesis, and reduced growth. In fish, high CO2 exposure interferes with neurotransmitter function, impaired olfactory sense, increased boldness, and loss of behavioral lateralization (Nilsson et al., 2012; Dixson et al., 2010), leading to overall impaired neurological and behavioral functioning. Ultimately, these disturbances can substantially increase the energetic costs of maintaining cellular homeostasis, resulting in physiological tradeoffs and shutting down some biological processes.
From a biological perspective, the US West Coast and Gulf of Mexico are two fundamentally different regimes with respect to surface water initial conditions that determine organismal exposure to OA. While the concentrations and values of biologically-relevant OA parameters in the Gulf of Mexico are much more favorable at present time, the OA conditions along the US West Coast have been demonstrated to already have a detrimental impact on some species (Bednaršek et al., 2014, Bednaršek et al., 2017). Since hypercapnia is defined as the exposures of 1000 uatm pCO2 for more than one month, some organisms are already experiencing chronic hypercapnia and low aragonite saturation state along the US West Coast. This condition is indicative of reduced habitat availability for some benthic and pelagic marine organisms, such as pteropods (Bednaršek et al., 2014, Bednaršek et al., 2017; Feely et al., 2016) and oysters (Waldbusser et al., 2015; Hales et al., 2017). In contrast, there is no subsurface hypercapnic exposure in the Gulf of Mexico. It is important to emphasize that some taxa in the upwelling regimes are expected to have developed acclimatization-adaptation strategies over longer periods of time to allow them for coping with hypercapnia/low Ω exposure. On the other hand, in the absence of unfavorable conditions that would influence long-term development of adaptation capacity, the organisms in the Gulf of Mexico are predicted to have higher sensitivity to small scale changes in hypercapnic/OA stress in the near-future. In this paper, we will compare the changing pHT and carbonate chemistry from the surface ocean to the hypoxic boundary (O2 ~ 60 µmol kg−1) for the West Coast of North America and Gulf of Mexico and examine how the two regions will evolve in the future under high-CO2 conditions.
Section snippets
Sampling and analytical methods
Detailed observations of carbonate system chemistry and other physical and chemical parameters were made along the western North American continental shelf (Fig. 1a). Vertical profiles of temperature, conductivity and pressure were obtained with a Seabird SBE 911plus CTD. Water samples from this cruise were collected in modified Niskin-type bottles and analyzed under ship-based or land-based laboratory conditions for DIC, total alkalinity (TA), pHT, oxygen, and nutrients. DIC was measured by
Modeling
Procedures for estimating changes in carbonate chemistry follow Cai et al. (2011) and Sunda and Cai (2012). Briefly, saturated dissolved oxygen concentrations of surface waters (pressure (P) < 15 dbar) were calculated as a function of temperature and salinity for the West Coast and Gulf of Mexico. The initial carbonate chemistry for surface waters was calculated using DIC and TA. Atmospheric pCO2 was set at five levels (400, 430, 550, 750, and 910 ppm) corresponding to present-day and year 2100
Cruise results
At all depths, the mean temperature, salinity, and aragonite saturation values in the Gulf of Mexico are significantly higher than the West Coast (Fig. 2). In contrast, Gulf of Mexico the mean dissolved oxygen was as much as 50% lower in the upper 20–30 m while pHT below 40 m is lower in West Coast waters. The 2013 West Coast cruise results showed evidence that surface seawater was close to equilibrium with respect to CO2 in the atmosphere in most regions, except for the nearshore upwelling
Comparison of the effects of anthropogenic CO2 on present and future acidification conditions in West Coast and Gulf of Mexico coastal waters
With increasing anthropogenic CO2 emissions over the next several decades, both pHT and aragonite saturation state are expected to decrease in surface and subsurface coastal waters and pCO2 will increase. At the surface, the percentage change in the carbon parameters are very similar for both regions even though the absolute change in aragonite saturation is much higher in the warmer waters of the Gulf of Mexico. For example, Table 1 and Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8 show comparisons
Discussion
Bjerrum plots of the carbonate species changes illustrate how the two ocean locations can be expected to respond under high-CO2 emissions (Fig. 9). Colder oceans with greater initial dissolved oxygen concentrations (e.g., the West Coast) experience larger increases in CO2 from surface to the hypoxic boundary and therefore have greater shifts to the left along the pHT scale of the Bjerrum diagram (Fig. 9a, b). This demonstrates how both waters start at similar pH conditions at the surface (Table
Biological effects of hypercapnia and other stressors
In the ecosystem with high RFs (US West Coast), which results in high non-linear pCO2 amplification, the hypercapnia effects will be magnified and accelerated compared to the system with lower RFs (Gulf of Mexico). As such, oceanic waters along the US West Coast will reach critical thresholds for hypercapnia much sooner, imposing negative effects to numerous groups of organisms and commercial fisheries. High Revelle factor-enhanced hypercapnia is especially vulnerable for the open ocean where
Conclusions
The decrease in pHT and aragonite saturation state, as well as the increase in pCO2 of subsurface coastal waters, from the combined effects of “classical” ocean acidification and oxidative acidification (i.e., respiration processes) is significantly enhanced by the higher RF and the enhancement of the respiration process in the colder waters of the West Coast relative to the Gulf of Mexico. Consequently, in colder waters we should observe greater seasonal variability and more rapid response to
Acknowledgements
This research was supported by the United States National Oceanic and Atmospheric Administration (NOAA), the National Science Foundation (NSF), and the National Aeronautics and Space Administration (NASA). We especially want to thank Libby Jewett and Dwight Gledhill of the NOAA Ocean Acidification Program and Dave Garrison of the National Science Foundation for their support. Nina Bednaršek was supported by the Pacific Marine Environmental Laboratory of NOAA and the NOAA Ocean Acidification
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