Benthic–pelagic coupling in the Gulf of Mexico hypoxic area: Sedimentary enhancement of hypoxic conditions and near bottom primary production

Continental Shelf Research 85 (2014) 143–152

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Benthic–pelagic coupling in the Gulf of Mexico hypoxic area: Sedimentary enhancement of hypoxic conditions and near bottom primary production Clifton C. Nunnally a,n, Antonietta Quigg a,b, Steve DiMarco a, Piers Chapman a, Gilbert T. Rowe a,b a b

Department of Oceanography, Texas A&M University, 3146 TAMU, College Station, TX 77843-3146, United States Department of Marine Biology, Texas A&M University at Galveston, 200 Seawolf Parkway, Galveston, TX 77553, United States

art ic l e i nf o

a b s t r a c t

Article history: Received 1 November 2013 Received in revised form 17 May 2014 Accepted 13 June 2014 Available online 1 July 2014

The seasonal bottom water hypoxia that covers large portions of the Louisiana continental shelf (USA) can extend far beyond the nutrient-rich Mississippi River plume. The hypoxia usually persists under surface-water that is all but depleted of nitrogen and phosphorous. Steep near-bottom gradients of NH4 þ during summer hypoxic conditions suggest that the sediments may become a net source of fixed nitrogen, potentially providing an important limiting nutrient to the system. Coupled measurements of benthic ammonium fluxes and water column NH4 þ profiles are combined to estimate turnover time of ammonium below the pycnocline. A tight, statistical relationship between photosynthetically active radiation (PAR) and NH4 þ reflects uptake by photosynthesis in the chlorophyll maximum, but utilization by nitrifiers and heterotrophic microbes could also be important at low levels of light, consuming oxygen (and thus contributing to hypoxia) and removing fixed nitrogen by denitrification. & 2014 Elsevier Ltd. All rights reserved.

Keywords: Benthic–pelagic coupling Nitrogen Nitrification Ammonium Hypoxia

1. Introduction In the northern Gulf of Mexico, the Mississippi and Atchafalaya Rivers deposit freshwater laden with anthropogenic nitrogen and phosphorous derived from agriculture across the entire mid-western United States. As a consequence of such extensive nutrient loading (Rabalais et al., 2002) and a strongly stratified water column (DiMarco et al., 2009; Wiseman et al., 1997), large areas of the sea floor are overlain by hypoxic waters. This predictable seasonal summertime hypoxia impacts food-webs, cycling of carbon, and the stoichiometric relationship between nutrients on the continental shelf (Dodds, 2006; Turner and Rabalais, 1994). The northern Gulf of Mexico hypoxic zone has increased in size since regular measurements began in 1985 (Rabalais et al., 1999; Turner et al., 2008). The geographic area is determined in part by total runoff (Wiseman et al., 1997), east–west wind persistence (Feng et al., 2012; Forrest et al., 2011) and river flow and associated nitrate loads (Turner et al., 2008). Bottom water hypoxia can extend to the west beyond the freshwater

n Corresponding author. Present address: Department of Oceanography, University of Hawaii at Manoa, 1000 Pope Road, Honolulu, HI 96822, United States. Tel.: þ 1 808 597 6009; fax: þ 1 808 956 8668. E-mail addresses: [email protected] (C.C. Nunnally), [email protected] (A. Quigg), [email protected] (S. DiMarco), [email protected] (P. Chapman), [email protected] (G.T. Rowe).

http://dx.doi.org/10.1016/j.csr.2014.06.006 0278-4343/& 2014 Elsevier Ltd. All rights reserved.

plume to regions where surface primary production is nitrogen limited (Quigg et al., 2011) and large amounts of sinking particulate organic matter (POM) are thus not produced. However, this region remains strongly stratified. Current paradigms of nutrient-enhanced coastal eutrophication resulting in hypoxia thus cannot explain these large regions of low bottom water oxygen concentrations. Lacking enhanced primary production at the surface, these areas must be subject to alternative processes that fuel and maintain hypoxia. Pelagic recycling of nutrients is rapid compared to benthic biogeochemical cycling (Billen, 1978). The lag time associated with benthic remineralization allows spring and early summer POM input to be available as recycled nutrients later in the year. In the case of the northern Gulf of Mexico hypoxic zone, benthic nutrient release can fuel phytoplankton growth at the end of the summer when surface waters become nitrogen limited (Quigg et al., 2011; Sylvan et al., 2006) and the euphotic zone deepens (Lehrter et al., 2009). While sediment nutrient regeneration and euphotic zone depth have both been estimated in numerous locations, they are rarely measured simultaneously and few direct comparisons have been attempted. Nitrogen limitation of primary productivity is evident in the western region of the GoMHZ (Quigg et al., 2011). Suspended particulates associated with river input are negligible in this region; this increases the penetration of photosynthetically active radiation (PAR) creating chlorophyll maxima near the bottom. In this western extremity of the hypoxic zone, the surface water is depleted of

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nitrogen, but phytoplankton growth in deep waters is ostensibly supported by nutrient regeneration in sediments (Lehrter et al., 2009; Murrell and Lehrter, 2011; Nunnally et al., 2013). The sediments are a source of ammonium that is preferentially scavenged by autotrophs and heterotrophs alike, resulting in competition among nitrifiers, heterotrophs and phototrophs for this nutrient. As a consequence between 25% and 50% of the total primary production in these circumstances is thought to be found beneath the pycnocline (Lehrter et al., 2009). Nitrification below the pycnocline consumes oxygen and could thus play a role in intensifying and prolonging hypoxia (Pakulski et al., 2000). The relative contribution of nitrification to ammonium removal can increase near the bottom of the photic zone (Ward, 2013; Ward et al., 1984); the nitrifiers could have a competitive advantage because phototrophs are light limited. Ammonium in the lower water column near the sediments would enhance oxygen depletion though nitrification and heterotrophic microbial respiration. Thus primary and secondary production utilizing ammonium may contribute to the POM pool in the near-bottom water (Azam

et al., 1983). All of these processes contribute to the systemic causes of hypoxia in the western regions of the Louisiana continental shelf. Sub-pycnocline photosynthesis adds dissolved oxygen to the depleted bottom layer; however oxygen budgets in Gulf of Mexico hypoxic zone provide little evidence that this contribution to bottom water oxygen is large enough to ameliorate hypoxia (Dortch et al., 1994; Rowe, 2001). It is our hypothesis that the regeneration of nitrogen by sediments, primarily ammonium, stimulates primary production beneath the pycnocline. This then provides a new source of organic matter which when respired works to maintain hypoxic bottom waters until stratification on the continental shelf breaks down. Due to the already depleted stock of dissolved oxygen the amount of this OM need not be great as long as it provides enough substrate to allow for a positive oxygen debt in sub-pycnocline waters. Our objective is to provide evidence of this mechanism at work using multiple data sets collected during 2004–2005 cruises of the Mechanisms Controlling Hypoxia (MCH) project to construct and validate a nitrogen budget incorporating previous research

Fig. 1. Map of Mechanisms Controlling Hypoxia study zones on the Louisiana continental shelf. Process oriented mooring stations are represented by black squares. Western study stations Zone C and Zone D are the focus of this study.

Fig. 2. Conceptual nitrogen budget of benthic–pelagic coupling with in the NGoM Hypoxic Zone. Listed are the measured stocks and flows along with important literature derived variables from within the MARS plume region. Boxes are the stock variable and arrows represent flow of nutrients between stocks. This represents the design of the budget as understood within the hypoxic plume region beneath the stratified surface layer.

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important to the fate of bulk nitrogen inventories. From this evidence we then propose a “simple” answer based on straightforward data that will help explain the prolonged hypoxia within the far-field region of the northern Gulf of Mexico (GoM) hypoxic zone.

2. Methods 2.1. Site and season selection The “Mechanisms Controlling Hypoxia” (MCH) project conducted a series of research cruises within the plume and at areas along the Louisiana continental shelf that are affected by seasonal summer hypoxia (Fig. 1). Cruises were scheduled in the spring and throughout the summer months to characterize the processes that play a role in the formation, and breakup of water column stratification and associated hypoxia (hypoxia.tamu.edu). In 2004 and 2005 processes measurements were made in near, mid and far-field regions of the northern Gulf of Mexico hypoxic zone; these include measurements of sediment fluxes of oxygen and nutrients and the calculation of primary productivity. The locations of the standard monitoring sites (A–D) were based on three habitat categories that typify the plume: brown water (A), green water (B) and blue water (C) (from Rowe and Chapman, 2002). The additional site, D, to the west is also blue water that can be hypoxic; it was added because C can be affected by nutrient-rich water when the plume is large during a wet year. Zone C is within an intermediate area of the Mississippi Atchafalaya River System (MARS) representing a green/blue transitory zone; prior to this study the Zone C location on the continental shelf experienced 50–75% annual hypoxia. In the far western areas (C 29.00031N, 92.00041W and D 29.20391N, 92.7061W, Fig. 1) a stratified water column prevents mixing, and this eventually leads to hypoxia (Rowe,

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2001), despite nitrogen limitation during this time of year. These latter two locations are appropriate for measuring the coupling of benthic nutrient regeneration with photosynthesis because the euphotic zone deepens relative to the plume region found at Zone A, and to a lesser extent, at Zone B (Fig. 1). Data is presented from seven cruises included in this study: April, June and August 2004 and March, May, July and August 2005. Sediment nutrient fluxes were measured in triplicate from each zone and paired with discrete water column samples used to evaluate chlorophyll-a content and primary production.

2.2. CTD profiles At all stations, a full-depth CTD cast was taken to within 1–2 m of the bottom using a SeaBird 911 CTD fitted with a SB43 oxygen probe mounted on a 12-bottle rosette. Discrete water samples were obtained from multiple bottles on each cast and analyzed for salinity (Guildline salinometer), dissolved oxygen (WOCE, 1991) and nutrients (nitrate, nitrite, phosphate, ammonia, urea and silicate) using standard autoanalyzer methods (WOCE, 1991); ammonia based on Harwood and Kühn (1970); urea based on Rahmatullah and Boyde (1980). Samples closer to the bottom were taken using a “Pogo” sampler, which consisted of four bottles mounted on a frame that tripped when a large plate suspended beneath made contact with the bottom. We estimate that this sampled to within 30–80 cm of the bottom. Bucket surface samples were also taken for nutrient and salinity measurements. Minimal detectable concentrations of the methods mentioned above were sub-micromolar for nitrate (0.041 mM), nitrite (0.012 mM), ammonium (0.057 mM), urea (0.075 mM), phosphate (0.025 mM) and silicate (0.127 mM). Individual nutrient analyses

Table 1 Flow values and literature sources used for nitrogen budget. Budget parameter Literature derived values

Nitrification PP N VMAX PP N KT Microbial N uptake Surface sinking POM Grazing N Kd

Measured values

Zone Zone Zone Zone Zone Zone

Value

Source 1

C NH4 þ efflux C phytoplankton N C bottom water [NH4 þ ] D NH4 þ efflux D phytoplankton N D bottom water [NH4 þ ]

0.008 lM N d 0.45 h  1 1.0 lM N 0.0002 lM N h  1 0.214 mM N m  3 d  1 1 mmol N m  2 d  1 0.0038 m  2 h  1

Pakulski et al. (2000) Goldman and Glibert (1983) Eppley et al. (1969) Wheeler and Kirchman (1986) Redalje et al. (1994) Dagg (1995) Gargett (1984)

1425 lmol m  2 d  1 0.017 mol N m  3 d  1 8.06 mol N m  3 d  1 914 lmol m  2 d  1 0.023 mol N m  3 d  1 6.30 mol N m  3 d  1

This This This This This This

study study study study study study

Table 2 Variability of bottom water oxygen concentration and nitrogenous sediment fluxes during 2004–2005 of MCH Project for Zones C and D. Mean sediment fluxes are reported in mmol m  2 d  1. Positive values indicate release by sediments and negative values indicate sediment uptake. Zone

C

Year

2004

2005

D

2005

Cruise

Month

[O2] (mg L  1)

Mean sediment fluxes NH4 (lmol m  2 d  1)

NO3

NO2

Urea

 367.3  915.4  80.6 6.1  80.0  45.5  189.3

9.1 968.7  95.2 21.9  7.1  52.2  141.7

1 2 3 4 5 6 7

April June August March May July August

4.13 1.69 1.48 2.67 2.59 2.47 0.19

1160.4 2568.7 863.4 159.6 719.2 663.4 483.6

58.9  65.5 43.3  482.4  131.6 225.0  225.2

6 7

July August

0.79 1.82

1837.59  91.97

176.88  249.04

 81.25  79.07

 20.90  101.89

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were reproducible to within 3% for all nutrients except ammonium which was reproducible to 6%. 2.3. Primary production 2.3.1. 14C primary production Photosynthesis versus irradiance relationships were determined using the small volume 14C incubation method of Lewis and Smith (1983). A calibrated Biospherical Instruments Model QSL-100 irradiance meter with a QSL-101 4π sensor measured quantum irradiance (mmol quanta m  2 s  1) in a photosynthetron. Temperature was kept constant with a circulating water bath set to ambient. Water samples were collected into acid-washed brown bottles and immediately assayed by spiking seawater with

14 C–sodium bicarbonate (final concentration¼1 mCi mL  1). Incubations lasted 30 min in July and August and 45 min in March and May at a range of irradiances from 5 to 1500 mmol quanta photons m  2 s  1. The reactions were terminated with buffered formalin (100 mL) and placed on a shaker table overnight with 50% HCl (1 mL) to purge off unincorporated label. After no less than 12 h, Ecolume scintillation cocktail (5 mL) was added to each vial and counted on a calibrated Beckman LS8100 Scintillation Counter. Triplicate (1 mL) samples for background (To) counts (with 100 mL of buffered formalin) and total (Tc) counts (with 250 mL of phenylethylamine and 5 mL of Ecolume scintillation cocktail) were prepared at the start of each incubation and kept at the same temperature as the samples in the photosynthetron. Dissolved inorganic carbon (DIC) in seawater was determined from

Fig. 3. Temporal variation of bottom water conditions in the far-field regions of the northern Gulf of Mexico hypoxic zone. (A) Bottom water oxygen concentration, ammonium and nitrate fluxes during 2004 MCH cruises 1–3 at Zone C. (B) Ammonium and nitrate concentrations of the bottom water during 2004 MCH cruises 1–3 at Zone C. (C) Bottom water oxygen concentration, ammonium and nitrate fluxes during 2005 MCH cruises 4–7 at Zone C. (D) Ammonium and nitrate concentrations of the bottom water during 2005 MCH cruises 4–7 at Zone C.

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Table 3 Integrated primary production values, depth of pycnocline and surface C:N ratios of western MCH zones. Primary production is divided into two calculated values for integrated production above the pycnocline and below the pycnocline. Zone

C

Year

2004

2005

D

2005

Cruise

Month

Primary production (g C m  2 d  1) Above

Below

Total

Pycnocline depth (m)

Surface C:N

1 2 3 4 5 6 7

April June August March May July August

1.10 0.03 0.53 0.44 0.03 2.20 0.32

3.42 0.52 2.03 0.73 0.35 0.96 2.38

4.52 0.55 2.55 1.17 0.38 3.16 2.71

– 2.5 6 9.5 8.5 17.5 6.5

4.1 8.5 4.8 – 4 6.3 19.6

6 7

July August

1.91 0.21

0.34 2.25

2.25 2.46

16 10

20 20

Fig. 4. Profiles of dissolved nutrients with depth in MCH Zones: (A) C (MCH cruises 2, 3, 5, 6 and 7) and (B) D (MCH cruises 6 and 7).

representative (Lohrenz et al., 1990, 1997) sites using a LiCor model LI6252 CO2 analyzer; the average DIC was 1.975 mmol C l  1 (Quigg et al., 2011). P–I curves were constructed by fitting the Chl a normalized data to the equation of Platt et al. (1980). Integrated primary production (g C m  2 d  1) was estimated by assuming a 12 h (March) or 14 h (May, July and August) photoperiod. Due to technical difficulties, when we were not able to calculate our own vertical attenuation coefficients, we used those of Lohrenz et al. (1990, 1997) for waters in the northern Gulf of Mexico. 2.4. Budget construction. A conceptual nitrogen budget was created and is represented by a diagram that tracks the flows and stocks of nutrients that could support primary productivity beneath the pycnocline and as such it ignores processes in the surface layer (Fig. 2). Our budget allows us to link measured environmental components (e.g. producer biomass, bottom water nutrient concentrations, etc.) using measured flows of nitrogen between these stocks of nitrogen that occur within the system (Fig. 3). Two key components central to our hypothesis are the flux of NH4 þ from the sediments to the overlying water (Nunnally et al., 2013) (summarized in Table 2) and the fate of NH4 þ integrated through the water column. In addition the concentrations of nitrogen were measured at discrete depths. Budget stocks (bottom water N concentrations and phytoplankton), flows (ammonium efflux, sinking PON, microbial N uptake, and literature sources are summarized in Table 2). The scope of our project did not allow for the itemized study of all processes that are important to the flow of nitrogen within the ecosystem and thus literature sources are used to fill in

the gaps of our knowledge. Studies in the northern Gulf of Mexico hypoxic zone have made concentrated efforts to understand the many facets of nitrogen cycling in our study area (Dagg and Breed, 2003) allowing us to limit uncertainty of measurements that are important to the accurate construction of our budget.

3. Results Parameters measured in Zones C and D were selected as the best combination of temporal and spatial variables (Table 1, Fig. 1) that might provide a clearer picture of the interaction between the sub-pycnocline water column and benthos providing a detailed basis for a budget (Fig. 2). Summer MCH cruises (MCH cruises 2, 3, 5, 6 and 7) occurred when surface waters were experiencing nitrogen limitation (low dissolved inorganic nitrogen (DIN):P ratios) accompanied by a significant increase in photic zone depth (Table 3). During late summer in the western regions of the MCH study area the chlorophyll maximum was frequently deeper than the pycnocline and strong nutraclines were measured (Fig. 4). 3.1. Profiles of nutrient concentrations The highest concentrations of inorganic nutrients on the western Louisiana continental shelf in Zones C and D (in Fig. 1) were near the bottom; they were almost depleted just below the pycnocline (Fig. 4). The highest nutrient concentrations at C and D were NH4 þ , with values that reached 40–60 mM adjacent to the sea floor (Fig. 4). The decline of nitrate and ammonium above the bottom was logarithmic at Zone C, reflecting a substantial

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Fig. 5. Integrated primary production for surface water above the pycnocline (white bars) and the deep mixed layer below the pycnocline (gray bars). (A) Integrated primary production at Zone C during 2004 MCH cruises 1–3. (B) Integrated primary production at Zone C during 2005 MCH cruises 4–7. (C) Integrated primary production at Zone D during 2005 MCH cruises 6 and 7. (D) Integrated primary production at Zone D during 2004 MCH cruises 6 and 7. Difference in sampling times was 3 days and 3 h for MCH cruises 6 and 7 respectively.

biological sink below the pycnocline. The curves explain 70% and 55% of the variations with depth at C for ammonium and nitrate, respectively. The profiles of nutrient gradients away from the sea floor for D were similar (Fig. 4B). The logarithmic relationships explain 97% and 76% of the variation with depth for ammonium and nitrate, respectively.

3.2. Phytoplankton primary production and biomass At Zone C mean bottom water phytoplankton biomass (4.17 1.5 mg-chl-a m  3) was twice as high as that measured at the surface (2.170.4 mg-chl-a m  3). The same trend was seen at D where bottom water phytoplankton biomass (5.671.1 mg-chl-a m  3) far exceeded that in the surface (1.770.3 mg-chl-a m  3). A single factor ANOVA revealed no significant difference between the mean of chl-a concentrations above or below the pycnocline for Zone C (p¼0.156). Zone D chl-a concentrations were significantly higher below the pycnocline (ANOVA, p¼0.002) (Fig. 5). Discrete measurements of summertime primary production at the surface and at the deep chlorophyll maximum in Zone C were nearly equal (0.59 7 0.22 (mean7standard error) and 0.64 7 0.38 g-C m  2 d  1, respectively). At the furthest west station (Zone D) primary production at the deep chlorophyll maxima (0.67 0.2 g-C m  3 d  1) exceeded that of nitrogen limited surface waters (0.4 70.1 g-C m  3 d  1) during summer months. Single factor analysis of variance (ANOVA) demonstrated no significant differences in the means for discrete measurements of primary production above and below the pycnocline (C: p ¼0.947, D: p ¼0.391). Depth integrated primary production was of greater magnitude beneath the pycnocline except during MCH cruise 6 in July of 2005 when the pycnocline reached a maximum study depth of 17.5 and 16 m in Zone C and D respectively. This difference was not a significant one however (ANOVA Zone C: p ¼0.143, Zone D: p ¼0.768). The ratio of sub-pycnocline to above-pycnocline (SP: AP) productivity in Zone C varied from lows in April of 2004 (3.1) and March of 2005 (1.7) when surface waters were not yet

nitrogen limited to a high of 16.5 in July of 2004 when the surface was N limited (Table 3). 3.2.1. Photosynthetically available radiation (PAR) PAR (average) measured mid-day in August at Zones C and D declined sharply as a function of depth with slightly more transparent water at the western site (not shown). Nonetheless, values at the bottom were 4.3% of that at the surface, or within the lower limits of the euphotic zone. An extinction coefficient of  0.16 m  1 can be estimated from the PAR gradient. The only instances when the 1% PAR level did not extend to the bottom of Zone C were April 2004 and March 2005 (not shown). In Zone D the PAR depth at the deepest sampled depth were 6% and 3% of surface PAR during July and August 2005. That is, at both C and D there was adequate light for photosynthesis during hypoxic conditions (summer) throughout the entire 20 m water column. 3.2.2. Stoichiometric relationships Carbon to nitrogen (C:N) ratios of phytoplankton from the surface waters west of Atchafalaya Bay during April and May of 2004 were 4.1 and 5.2 respectively (Table 3), or less than the expected Redfield Ratio of 6.625, indicating that nitrogen was not limiting during the earliest parts of the hypoxic season. These C:N ratios eventually exceeded the Redfield Ratio, reaching 8.3 in June and 9.5 in July. C:N decreased in August, falling back to values similar to May C:N of 4.8 most likely due to mixing events that redistributed nitrogen throughout the water column. In 2005 a similar scenario of fluctuating C:N in Zone C with low (nitrogen replete) values occurring in May and July but rising into nitrogen limitation in August. Zone D showed considerably more variability, but again the C:N ratio was much higher than Redfield in both months at certain stations. May and July C:N ratios were taken from mean values of particulate organic carbon (POC) and particulate organic nitrogen (PON) measured by Sylvan and Ammerman (2013). Carbon to phosphorous (C:P) and nitrogen to phosphorus (N:P) ratios were exceptionally high in May (1946 and 345, respectively). By July the

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Fig. 6. (A) Ammonium concentration as a function of PAR below the pycnocline at C and D in August 2005. (B) Ammonium concentration as a function of depth at C and D during August 2005.

Table 4 Hypothetical vertical mixing constants in m  2 h  1 (0.0038 ¼0.01 cm  2 s  1) and resultant vertical fluxes based on the gradient a C between ca. 10 and 20 m depth (column 2), the resultant estimated biological uptake over that interval (column 3), along with that equivalent value in mg N m  2 h  1. K values

0.00038 0.001 0.0019 0.0038 0.0067

Mixing rates

0.002 0.0055 0.01 0.02 0.037

Utilization (mM m  2 h  1)

mg N m  2 d  1

0.036 0.033 0.028 0.018 0.001

12 10.8 9.4 6 0

C:P and N:P decreased by an order of magnitude (204 and 21, respectively), yet they were still above the Redfield Ratio, similar to other studies in the western regions of the GoMHZ (Quigg et al., 2011; Sylvan et al., 2006). 3.2.3. Ammonium concentrations Ammonium concentrations measured in Zone C during CTD casts for PAR followed an inverse relationship (Fig. 6A): high values of 45 and 60 mM occurred when light levels were below ca. 5%, whereas NH4 þ virtually disappeared at the surface when PAR was high. Ammonium below the mixed layer or pycnocline (5.7–10.7 m) declined exponentially as PAR increased toward the surface (Fig. 6B). 3.2.4. Ammonium turnover times in the sub-pycnocline water column The turnover time of the total stock of ammonium can be estimated from water column concentrations and the rate at which it is added at the sea floor (Nunnally et al., 2013). Graphical integration under the curves at Zones C and D between the sea floor and 10 m, the approximate depth of the pycnocline, gives 355 and 190 mM NH4 þ m  2 at C and D respectively, equivalent to 4970 and 2660 mg N m  2. Dividing these values by the mean 1 inputs (0.91 and 0.7 mM NH4 þ m  2 d ) gives turnover times of 391 and 271 days for C and D respectively. 4. Discussion 4.1. Nitrogen budget in the water column The concentrations and dynamics of ammonium in the water column are a function of release from the bottom, vertical mixing,

and biological uptake. The latter can be undertaken by photosynthetic phytoplankton, nitrifying bacteria or heterotrophic microorganisms. This general process can be expressed by the following: ∂½NH4 þ =∂z; t ¼ Input from the bottom–vertical mixing–uptake by the biota ð1Þ Assuming there is no change in the vertical gradient in time, and integrating both sides, results in the following: Input from the bottom ¼ vertical mixing þ uptake by the biota

ð2Þ

where vertical mixing ¼ kðammonium gradient over the depth intervalÞ=depth interval

ð3Þ

The nitrogen budget is centered on two principal variables: ammonium (NH4 þ ) input from the sediment community as determined from ship-board incubations and the declining gradient of NH4 þ away from the sea floor up to the pycnocline (Fig. 4). The transfer of nutrients cannot ignore certain physical parameters, even though we chose to describe the system as it exists below the pycnocline. The gradient of decreasing nutrients with increasing distance above the sea floor (source) is logarithmic and indicates that nutrient loss is not due to mixing alone (which would be linear), but has a biological component as well (Fig. 2). As such we chose to parameterize the vertical flux as Fickian diffusion (eddy mixing) using the following equation:
 d NH4 þ =dt ¼ 0 ¼ Input from sea floor–vertical eddy mixing–uptake by biota mM n h io

 1 2 2 1 NH4 þ m  2 d ¼ k d NH4 þ =d z –mM NH4 þ m  2 d ; where the integral of themixing term is 
 
 K d NH4 þ bottom  NH4 þ pycnocline =depth interval

ð4Þ

where Kd is a mixing coefficient (Gargett, 1984). The input from the sea floor is taken from Nunnally et al. (2013). We know neither the vertical mixing nor the uptake rate, but we can consider the effects of a range of mixing constants. Knowing the input, we can estimate the range of uptake rates by subtracting the vertical transfer attributable to a range of mixing rates from the input (Table 4). The Zone C location is utilized because it had the highest ammonium values. If the mixing were slow, then the uptake would be high, and vice versa. If mixing exceeds uptake, then the gradient is obliterated, as is commonly observed in the surface mixed layer. These values would support anywhere from zero up

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to 72 mg C m  2 d  1 fixed by photosynthesis On the other hand, if the ammonium were nitrified, the following might be assumed, using 0.018 mM NH4 þ from Table 1: ½mM NH4 þ m  2 h

1

 ½24 h=day ½1:5 mMO2 =mM NH4 þ 

¼ ½0:65 mM O2 m  2 d

1



The rates at Zone D would be proportionately lower because the gradient is lower. There were also gradients above bottom of nitrate (Fig. 4). However, Nunnally et al. (2013) measured a net loss of nitrate to the sediments in sediment incubations at sites in Zone A–D (see Fig. 1). The gradient observed may reflect initial nitrification (Ward et al., 1984; Pakulski et al., 2000) in dark bottom water and surficial sediments where oxygen is available, followed by denitrification to nitrous oxide and nitrogen gas (Rowe et al., 2002; Seitzinger et al., 1993). 4.2. Benthic–pelagic coupling The original suggestion that sediment community nutrient regeneration was important to continental shelf productivity, now referred to as benthic–pelagic coupling (¼BPC) (Rowe et al., 1975), was based on ammonium gradients in the bottom water across a broad area of the eastern US. The flux from the sea floor was estimated from calculations of vertical mixing up along the gradient from the sediments to the euphotic zone. But those original estimates lacked direct measurements of the source term, unfortunately. Substantial concentrations of ammonium had been observed in estuaries (Nixon, 1981), but rarely on continental shelves (Lin et al., 2011). Nonetheless, it is now recognized that nutrients are regenerated by sediments that fuel primary production in the water column on a wide variety of shallow continental shelves (Billen, 1978; Hopkinson Jr., 1987; Rowe et al., 1977, 1975), as well as estuaries (Gilbert et al., 2013; Nixon, 1981). In strongly stratified water columns however the interplay of the benthic and pelagic can be discretely de-coupled by the pycnocline (Carpenter and McCarthy, 1975), but benthic remineralization could be supplying nutrients to sub-pycnocline pelagic production when the euphotic zone penetrates the pycnocline, as observed at Zones C and D on the Louisiana continental shelf. In fact, previous model simulations from the Gulf of Mexico hypoxic zone, cycling of organic matter in sediments predict ammonium efflux can support 25–60% of primary production on the shelf (Eldridge and Morse, 2008). More recent studies to the contrary suggest that measured benthic ammonium efflux estimate that o10% of water column primary production could be supported (Lehrter et al., 2011), but this depends on where and when such a comparison (the river plume versus BPC) is made. Our budget estimates based on measured benthic ammonium efflux could support 76 and 59 mg C m  2 d  1 of primary production during the late summer months in Zones C and D, respectively. Recent studies have shown that although nitrate is abundant in bottom waters over the Texas–Louisiana shelf, it is consumed by sediments which are net producers of ammonium (Lehrter et al., 2011; Lin et al., 2011; Nunnally et al., 2013). Phosphorus contributions to BPC are nil because sediments appear to be a net sink for P in these western regions (Nunnally et al., 2013). Such sequestration could potentially contribute to phosphorus limitation (Quigg et al., 2011; Sylvan et al., 2006). Silicate, another important phytoplankton nutrient, was continually released from sediments (Lehrter et al., 2011; Nunnally et al., 2013) and was not limiting within the sub-pycnocline water mass. In ecosystems characterized by strong upwelling, benthic fluxes can be substantial but their relative importance compared to the nitrogen supplied by the upwelling remains relatively small (Bailey and Chapman, 1991; Calvert and Price, 1971; Chapman

Fig. 7. Conceptual diagram of ecosystem processes for far West regions of the Gulf of Mexico Hypoxic Zone with emphasis on sub-pycnocline mechanisms that enhance productivity and maintain bottom water hypoxia. PAR arrow represents photosynthetically active radiation. Arrow outside the box represents the changing position of the pycnocline in Zones C and D, showing maximum, minimum and average depth encountered during this study. The black arrows denote the direction of oxygen and nutrient exchange by the sediments.

and Shannon, 1985; Rowe et al., 1977). Conversely, off central Chile sediments can be an important source of nitrogen for the water column during El Nino when the upwelling shuts down (Graco et al., 2006). In the Gulf of Mexico coastal eutrophication is associated with the delivery of freshwater and dissolved nutrients from MARS springtime runoff. Decades of monitoring have now demonstrated that a large hypoxic zone is maintained well beyond obvious fluvial influences (Rabalais et al., 2007; Turner et al., 2008), despite clear evidence of nutrient limitation in the surface waters west of the nutrient-rich plume (Quigg et al., 2011; Sylvan et al., 2006, 2007). The nutrient limitation in surface waters can be eased when the pycnocline deepens, as in July 2005 (DiMarco et al., 2009), thus stimulating productivity throughout the water column (Table 3). If such processes are frequent, the “blue” (minimal surface productivity and increased light penetration) western shelf habitat might be dominated by subsurface processes rather than the plume (Fig. 1, sites A and B) with high levels of nitrate. Suboxic conditions can diminish the capability of sediments to remove nitrogen through the nitrification/denitrification couple, returning fixed N to the lower water column as ammonium. This retention of reactive nitrogen is important because current strategies for ameliorating hypoxia in the Gulf of Mexico focus on reducing riverine N loads in the hopes of reducing eutrophic conditions. The processes inferred in this study illustrate that benthic–pelagic coupling is an important loop that leads us to revisit the Rowe and Chapman (2002) conditions that must be satisfied for hypoxia to occur beyond the plume: intense stratification, alternative sources of nutrients, a deep euphotic zone and minimal transfer of nutrients to the surface layer. 4.3. Conclusion Our revised conceptual diagram of these features important for far-field regions of the northern Gulf of Mexico hypoxic zone (Fig. 7) illustrates potential contributions of the benthos and the sub-pycnocline water column to hypoxic mechanisms. Incorporated into Fig. 7 are the findings of several studies have showing (1) net release of ammonium and silicate by sediments in this region (Lehrter et al., 2011; Lin et al., 2011; Nunnally et al., 2013), (2) increased PAR levels in western Louisiana shelf hypoxic areas

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(Dortch et al., 1994; Lehrter et al., 2009) and (3) the physical forcing of shelf waves and river induced stratification (DiMarco et al., 2009; Forrest et al., 2011); all are needed to sustain hypoxic bottom waters. Analysis of phytoplankton concentrations and integrated primary production in this study revealed the importance of pycnocline depth as a factor controlling the distribution of nutrients. The fate of DIN released by sediments is not important as the three potential pathways of uptake enhance bottom water hypoxia. Heterotrophic uptake by microbes and nitrification will consume oxygen beneath the pycnocline. Phytoplankton growth stimulated by ammonium will provide new organic matter for respiration but not be of sufficient magnitude to reduce hypoxic stress. Additionally the clear water in late summer within this region releases phototrophs of competitive interactions with nitrifying bacteria for ammonium. Thus the simplest answer with the fewest assumptions, per Occam's Razor, is that nutrient release by sediments stimulates primary production fueling organic matter respiration prolonging hypoxia in the far-field regions of the northern Gulf of Mexico hypoxic zone.

Authors contribution C.C.N. conducted all the sampling at sea in dark incubations of his design, made all the flux calculations, interpreted all the flux data and wrote the initial draft of this ms. A.Q. measured the phytoplankton standing stocks, light and primary productivity. S.D.M. was the MCH PI and authored the physical interpretations. P.C. was in charge of sea water chemistry in MCH. G.T.R. suggested the original sampling pattern (as in Rowe and Chapman (2002)) utilized in the MCH project, provided the shipboard incubation apparatus and parameterized the relationships between water column concentrations and sediment fluxes.

Acknowledgments We would like to acknowledge the Captain and crew of the R/V Gyre for their support during seven spring and summer cruises in the Gulf of Mexico. A review by Daniel C.O. Thornton and two anonymous reviewers helped tremendously with the quality of this manuscript. Hard work at sea and in the lab by Federico Alvarez provided invaluable information concerning primary production. It is also important to note the tireless effort by our trusted data manager Matt Howard who compiled mountains of data that were disseminated for our use. Chris Schmidt at GERG measured the nutrients. Essential to our work was the help of students and colleagues from Texas A&M University at Galveston and Texas A&M University. This work was funded by two grants from the NOAA Center for Sponsored Coastal Research (NA03N0S4780039 and NA06N0S4780198) (NGOMEX Contribution no. 194). References Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A., Thingstad, F., 1983. The ecological role of water-coulmn microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263. Bailey, G.W., Chapman, P., 1991. Short-term variability during an anchor station study in the southern Benguela upwelling system: chemical and physical oceanography. Prog. Oceanogr. 28, 9–37. Billen, G., 1978. A budget of nitrogen recycling in North Sea sediments off the Belgian coast. Estuar. Coast. Mar. Sci. 7, 127–146. Calvert, S.E., Price, N.B., 1971. Upwelling and nutrient regeneration in the Benguela Current, October, 1968. Deep Sea Res. Oceanogr. Abstr. 18, 505–523.

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