Plankton community respiration, net ecosystem metabolism, and oxygen dynamics on the Louisiana continental shelf: Implications for hypoxia

Continental Shelf Research 52 (2013) 27–38

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Research papers

Plankton community respiration, net ecosystem metabolism, and oxygen dynamics on the Louisiana continental shelf: Implications for hypoxia Michael C. Murrell n, Roman S. Stanley, John C. Lehrter, James D. Hagy III US Environmental Protection Agency, Gulf Ecology Division, 1 Sabine Island Drive, Gulf Breeze, FL 32561, USA

a r t i c l e i n f o

abstract

Article history: Received 29 November 2011 Received in revised form 8 August 2012 Accepted 25 October 2012 Available online 7 November 2012

We conducted a multi-year study of the Louisiana continental shelf (LCS) to better understand the linkages between water column metabolism and the formation of hypoxia (dissolved oxygen o 2 ml O2 l  1) in the region. Water column community respiration rates (WR) were measured on 10 cruises during spring, summer and fall seasons from 2003 to 2007 at multiple sites distributed across the Louisiana continental shelf, overlapping the region where bottom-water hypoxia occurs. We found consistent broad scale patterns in WR rates that followed depth and salinity gradients across the shelf. Observed WR rates were highest at low salinity inner shelf stations (o 30 m depth) and decreased with increasing water depth. Surface waters had higher WR rates than bottom waters, a pattern most pronounced near the Mississippi river during spring and early summer. Surface water WR rates were highest in eastern transects and decreased westward; a trend that was not evident in bottom waters. WR tended to be higher in spring and summer compared to fall months, but overall the seasonal variability was small. We combined the WR rate measurements with contemporaneous measurements of phytoplankton productivity rates (reported in Lehrter et al., 2009, Continental Shelf Research, 29: 1861–1872) to estimate net water column metabolism. There was consistent evidence of net heterotrophy, particularly in western transects, and in deeper waters (4 40 m depth), indicating a net organic carbon deficit on the LCS. We offer a simple scale argument to suggest that riverine and inshore coastal waters may be significant sources of organic carbon to account for this deficit. This study provided unprecedented, continental shelf scale coverage of heterotrophic metabolism, which is useful for constraining models of oxygen, carbon, and nutrient dynamics along the LCS. Published by Elsevier Ltd.

Keywords: Northern Gulf of Mexico 281N to 29.51N 891W to 93.51W Primary Production

1. Introduction Human activities have altered coastal ecosystems via increased nutrient loading and organic matter production (i.e., cultural eutrophication) (NRC, 2000). Hence, understanding and quantifying the metabolic balance of coastal systems is of critical interest to scientists and policy-makers, particularly in developing robust global carbon budgets (Smith and Hollibaugh, 1993; Gattuso et al., 1998; Cai, 2011). One acute consequence of cultural eutrophication, is the formation of hypoxic (dissolved oxygeno2 ml O2 l  1) or anoxic (no dissolved oxygen) subsurface waters in coastal and estuarine systems across the world (Diaz and Rosenberg, 2008). A persistent lack of oxygen can fundamentally alter food webs by reducing the survival of many aquatic animal species (Breitburg et al., 2009). The Louisiana continental shelf (LCS) has been a region of sustained interest over the past 25 years due to the formation of

n

Corresponding author. Tel.: þ1 850 934 2433; fax: þ1 850 934 2401. E-mail address: [email protected] (M.C. Murrell).

0278-4343/$ - see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.csr.2012.10.010

summer hypoxia over large regions of the shelf (reviews: Rabalais et al., 2007; Dagg et al., 2007; Dale et al., 2009; Bianchi et al., 2010). The occurrence of hypoxia on the LCS has been attributed to a confluence of physical and biological factors including high freshwater flow and nutrient loads from the Mississippi– Atchafalaya river system (Goolsby et al., 1999), high phytoplankton production (i.e., eutrophication) in plume waters (Lohrenz, 2008; Lehrter et al., 2009), and strong density stratification caused by the freshwater plume (Wiseman et al., 1997; Hetland and DiMarco, 2008) that isolates bottom waters from the atmosphere. A portion of this enhanced productivity sinks to bottom waters (as phytoplankton cells or fecal pellets), where microbial decomposition of this organic matter consumes oxygen at a rate faster than it can be resupplied from atmospheric or lateral exchanges. Several prior studies have developed carbon budgets for the Mississippi river plume region and the linkage to hypoxic water mass formation across the shelf (Breed et al., 2004; Green et al., 2006; Dagg et al., 2008; Guo et al., 2012). However, only a few budgets have extended westward beyond the immediate Mississippi river plume to include the wider shelf region where hypoxia is

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M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

the region that routinely becomes hypoxic during summer (Rabalais et al., 2007; http://gulfhypoxia.net). At each station, water column profiles of temperature, salinity, depth, and dissolved oxygen (O2) were measured with a Seabird 911 CTD system. The pycnocline was determined as the depth of ¨ al ¨ a¨ Frequency (Pond and Pickard, 1983) maximum Brunt–Vais calculated from the CTD profiles. Water samples were collected in 10 l Go-Flow (during 2002–2006) or 10 l Niskin (during 2007) bottles. Samples were collected for a suite of standard water quality constituents (USEPA 2007), but only chlorophyll a (chl-a) data will be presented here as context for the respiration measurements. During one cruise (Sept–Oct 2005) salinity and dissolved oxygen were measured on bottle-collected water using a YSI salinometer and an Orion O2 meter (in situ temperature not measured). Samples for chl-a were filtered (100–500 ml) onto GF/F filters and frozen at 70 1C until analysis. In the laboratory, chl-a was extracted with sonication in buffered methanol (Jeffrey et al., 1997). Extract fluorescence was measured on a Turner Designs TD 700 fluorometer with optical filters specific for chl-a (Welschmeyer, 1994), and calibrated using a commercially available standard (Sigma Chemicals). Samples for plankton community respiration (WR) measurements were collected from several depths in the water column (surface and bottom minimum) into acid-cleaned 300 ml BOD bottles. Surface samples were collected within the top 1 m of the water column and bottom samples were collected within 2 m of the sediment water interface. The BOD bottles were filled first, before

observed (Bierman et al., 1994; Scavia et al., 2003). These existing budgets all predict a strong east–west gradient in heterotrophic metabolism, largely reflecting the expected westward movement of organic matter produced in the Mississippi river plume. The purpose of this study was to characterize spatial and seasonal patterns in water column plankton community respiration rates (WR) across the LCS and to estimate oxygen turnover rates in sub-pycnocline waters. Further, we examined spatial and seasonal patterns in empirical measurements of respiration in comparison with several hypoxia models. Finally, we included primary productivity data previously reported in Lehrter et al. (2009) with contemporaneous respiration measurements to estimate net water column metabolism. This study is part of a larger US EPA research program, which include companion studies describing coupled sediment–water column respiration rates (Murrell and Lehrter, 2011), and sediment nutrient and carbon fluxes (Lehrter et al., 2012).

2. Methods A series of 10 cruises were conducted from June 2003 to August 2007 spanning the Louisiana continental shelf from the Mississippi river outflow to westward of the Atchafalaya river outflow (Fig. 1). Over the study, over 500 stations were sampled, with 22 to 81 stations per cruise, and depths ranging from ca. 5 to 100 m (Table 1). The vast majority of stations were located within

X M K C J

I

H

G

F

E

B

A

D

Fig. 1. Map of the Louisiana continental shelf showing stations oriented along inshore–offshore transects adapted from the LUMCON sampling design. The polygon depicts the region where hypoxia has been historically observed during annual July surveys (Walker and Rabalais, 2006). The stations are grouped into transects, denoted by the letters X, M, A, etc.

Table 1 Summary of cruise dates, the depth range of samping, the surface water temperature and salinity ranges, the number of WR and GPP stations, and the transects occupied. See Fig. 3 for station locations. Cruise dates

Depth range

Salinity range

Temp. range (1C)

12–19 Jun 2003 6–16 Nov 2003 2–6 Apr 2004 22–30 Mar 2005 29 Sep–7 Oct 2005 13–17 Apr 2006 6–11 Jun 2006 6–11 Sep 2006 2–7 May 2007 19–24 Aug 2007

7.7–171 6.8–175 6.4–51 3.2–345 5.4–305 6.5–67 7.3–134 6.6–110 7.0–116 6.0–108

0.2–35.6 1.4–35.9 0.2–29.7 0.2–36.6 2.6–36.1 3.2–36.5 1.1–36.1 6.6–36.4 0.9–36.5 5.4–34.7

24.8–29.4 21.0–25.8 14.8–22.9 11.3–22.7 nd 18.4–22.5 25.6–30.7 29.0–31.7 18.7–26.7 29.8–31.5

Total

#WR stations 30 45 22 38 37 43 74 81 81 78 529

#GPP stations

Transects occupied

– – – 23 32 36 56 69 59 66

M, A, M, A, M, A, M, A, X, M, X, M, X, M, X, M, M, A, X, M,

341

C, D, E, F, H B, C, D, E, F, G, B, C, D, E, F C, D, F, H, J A, B, C, D, E, F, A, B, C, D, E, F, A, B, C, D, E, F, A, B, C, D, E, F, B, C, D, E, F, G, A, B, C, D, E, F,

H, J

G, H, J G, H, J G, H, I, J, K G, H, I, J, K H, I, J, K G, H, I, J, K

M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

drawing samples for other water quality constituents, using a length of Tygons tubing inserted into the bottom of bottle and allowing water to overflow by 1–2 volumes before capping, taking care to expel all bubbles. After initial O2 measurements, samples were placed in a darkened incubator that maintained surface water temperatures using water supplied continuously from the ship’s hull pump. The incubator temperature was routinely monitored and typically fell within 1–2 1C of surface water temperature based on comparisons with CTD data. Concentrations of O2 were measured initially and after 24 h using an Orion 862 A O2 sensor probe. The probe included a stirrer mechanism and a beveled fitting that matched the opening of the BOD bottles. The O2 sensor was calibrated against water–saturated air, corrected for temperature and barometric pressure. To evaluate sensor drift, O2 readings in water–saturated air were made several times per day, and recalibrated if readings varied 42% from initial conditions. However, sensor stability was generally excellent, typically requiring no recalibration over the course of the cruise. WR was calculated as the change in O2 over time, expressed in units of mmol O2 m  3 d  1. The values reported are averages of duplicate BOD bottle incubations; the coefficient of variation among duplicates averaged 27% (data not shown). To account for small differences between the incubator temperature and ambient water temperature, WR rates were adjusted assuming Q10 ¼2, as: WR ¼ WRi  2ðTT i Þ=10 , WRi is the respiration rate at incubator temperature (Ti), and T is the ambient water temperature measured by the CTD. While typically a small correction (less than 710%), it helped reduce bias in WR rate measurements. During the Sept–Oct 2005 cruise, CTD temperature data were not available, so the raw measurements were reported without temperature correction. The detection limit for this method was  2 mmol O2 m  3 d  1. About 15% (n¼196) of the measurements were below detection, most of which occurred in offshore high salinity bottom waters. We experimented with several parametric and non-parametric means of handling the censored data (Helsel, 2005), all of which produced very similar results. Based on the observation that non-censored WR rates were log-normally distributed, we opted to replace non-detects with simulated values drawn from the left tail of a log-normal distribution fitted to the non-censored data, reasoning that this approach should result in negligible bias in the resulting statistical analyses. Respiration rates were integrated through the water column assuming that the pycnocline defined the boundary between surface and bottom layers. At most sites, there was a clearly definable pycnocline; at sites with no clearly definable pycnocline, the surface and bottom layers were defined as the upper and lower half of the water column, respectively.

29

The primary productivity data, originally reported in Lehrter et al. (2009), were calculated from 24 h 14C incubations, thus considered to be net productivity rates. Gross primary productivity was estimated by adding a basal phytoplankton respiration rate term (Flynn, 2005), as 10% of the maximum (light saturated) 14C uptake. Net water-column metabolic rates were calculated as the sum of the integrated gross primary production (GPP) and the integrated water column respiration (IWR), assuming equivalent C:O stoichiometry (i.e., RQ¼PQ¼ 1). Net metabolic rates were evaluated statistically using simple error propagation techniques (Bevington, 1969; Lehrter and Cebrian, 2010), and deemed statistically significant if the 95% confidence intervals did not overlap zero.

3. Results 3.1. Freshwater flow and salinity distributions Over the 4 year span of this study, freshwater flow from the Mississippi and Atchafalaya rivers (Fig. 2) generally followed long term seasonal trends characterized by peak flows during winter and spring and low flow during summer and fall. Notable exceptions included an above average flow period from Sep. 2004 to Feb. 2005, which was followed by a prolonged ( 18 month) low-flow period from Mar. 2005 to Sep. 2006. For example, the 2006 spring (Jan.–Mar.) flow, only 64% of normal, was the 3rd lowest spring flow in the 57-year record. The study also spanned a period of intense meteorological activity, particularly during summer 2005, when Hurricanes Katrina (August) and Rita (September) traversed the eastern and western reaches of the LCS, respectively. Maps of water column average salinity (Fig. 3) broadly reflected the prevailing flow regime; with salinity contours deflecting inshore during low flow and offshore during high flow. Domain-average salinity calculated from the interpolated grids in Fig. 3 ranged from a low of 32.4 in March 2005 reflecting the recent flood, to a high of 34.5 in April 2006 reflecting the drought (data not shown). Despite the large variation in freshwater flow, the effect on the shelf-wide salinity distributions was subtle, indicating a persistent inshore–offshore gradient. 3.2. Plankton community respiration A total of 1289 WR rate measurements were made at 529 stations distributed across the Louisiana continental shelf (Table 1). When summarized by cruise (Table 2), mean WR rates ranged from 6.4 to 16.6 mmol O2 m  3 d  1 in surface waters, 4.5–11.4 mmol O2 m  3

40

1950-2007 average

Flow (X 1000 m3 s-1)

This study

30

20

10

0 Jan

Jul 2003

Jan

Jul 2004

Jan

Jul 2005

Jan

Jul 2006

Jan

Jul

Jan

2007

Fig. 2. Freshwater flow during study (solid line) from the Mississippi–Atchafalaya river system in relation to long-term averages (1950–2007, shaded area). Data are monthly averages of the combined flow from the Mississippi river at Tarberts Landing and Atchafalaya river at Simmsport from U.S. Army Corps of Engineers gaging stations. Arrows denote timing of cruises. Vertical lines separate calendar years.

30

M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

30°N

30 29°N

35

35 28°N

Fig. 3. Contour plots showing the distribution of salinity on the LCS during each cruise. Contours represent water column average salinity. The symbols denote sampling stations. (A) June 2003, (B) Nov 2003, (C) Apr 2004, (D) Mar 2005, (E) Sep-Oct 2005, (F) Apr 2006, (G) June 2006, (H) Dept 2006, (I) May 2007 and (J) Aug 2007.

d  1 in mid-depth waters and 4.9–8.7 mmol O2 m  3 d  1 in bottom waters. WR rates in all water layers tended to be higher in spring and summer and lower in the fall.

The spatial and seasonal patterns in WR rates were examined by binning data by transect (Fig. 4A) and water depth (Fig. 5A), month (Fig. 6A), and salinity (Fig. 7A). The data were further split

M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

31

Table 2 Plankton community respiration (WR) rate measurements summarized by cruise for surface, mid-depth, and bottom waters on the Louisiana continental shelf. Included are means, standard errors, maxima, and the number of observations. Minima were not included due to below detection data. Units are mmol O2 m  3 d  1. Seasonal and grand means (7SE) were calculated from cruise means. Cruise

Jun 2003 Nov 2003 Apr 2004 Mar 2005 Sep–Oct 2005 Apr 2006 Jun 2006 Sep 2006 May 2007 Aug 2007 Spring (Mar–May) Summer (Jun–Aug) Fall (Sep–Nov) All data

Surface

Mid-depth

Bottom

Mean

SE

Max

N

Mean

SE

Max

N

Mean

SE

Max

N

12.7 6.3 16.6 13.6 6.4 9.6 14.8 8.7 11.8 10.8 12.9 12.7 7.1 11.1

(1.4) (0.6) (1.8) (1.5) (0.9) (1.2) (1.8) (0.8) (1.1) (0.8) 7 1.5 7 1.2 7 0.8 7 1.1

33.4 18.6 39.5 39.4 25.0 36.6 99.3 40.1 42.1 30.0

29 42 21 37 35 43 71 79 75 78 176 178 156 510

11.4 5.7 10.3 10.1 4.9 4.5 6.0 6.3 7.7 7.9 8.2 8.4 5.6 7.5

(1.7) (0.5) (2.5) (1.6) (1.3) (0.7) (1.2) (1.2) (2.2) (2.3) 71.4 71.6 70.4 70.8

40.0 12.6 69.9 33.8 35.3 13.8 19.7 20.3 38.8 21.2

29 31 29 33 27 22 22 25 23 10 107 61 83 251

8.7 5.2 8.0 7.2 4.9 6.9 7.6 6.9 6.5 7.8 7.1 8.0 5.7 7.0

(1.4) (0.4) (1.9) (1.6) (0.7) (0.9) (0.8) (0.9) (0.8) (0.7) 7 0.3 7 0.3 7 0.6 7 0.4

30.0 12.8 35.3 46.6 16.2 38.4 43.7 64.1 27.8 25.6

30 45 22 38 37 43 74 81 81 77 184 181 163 528

22

25 Surface Layer

WR (mmol O2 m-3 d-1)

Bottom Layer

20 53 36

15

55

44

10

19

28

50 35

39

49 31

43

5

0 21

GPP, IWR, NEM (mmol O2 m-2 d-1)

350

Production 19

Respiration

250

31

NEM

35 29

150

30

17

32

26

30

G

H

23

29

I

J

19

50 -50 -150 -250 -350

X

M

A

B

C

D

E F Transect

K

Fig. 4. Transect bin averages of: (A) plankton community respiration (WR) in the surface layer (shaded bars) and the bottom layer (open bars), and (B) integrated gross primary production (GPP, shaded bars), respiration (IWR, open bars), and net metabolism (NEM, symbols). Solid symbols indicate that net metabolism was statistically distinguishable from zero, as described in text. Error bars are standard errors. The number of observations for each bin is included.

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M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

20

20 63

2005 Bottom Layer

15

181 105

61

10

94

5

WR (mmol O2 m-3 d-1)

WR (mmol O2 m-3 d-1)

Surface Layer

Production Respiration NEM

350 250

64

74

36

15

2003 2006 99

2007

2005 2006

2005

2003

Surface Layer Bottom Layer

77 91

10

22

41

5

35

133 71

300

46 56

150 50 -50 -150 -250 -350

2007

0

0-10

10-20

20-30 Depth Bin

30-40

>40

GPP and IWR (mmol m-2 d-1)

GPP and IWR (mmol O2 m-2 d-1)

0

2004 2006

36

200

66

80

56 59

23

100

21

0 -100 Production Respiration NEM

-200 -300 Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Month Bin Fig. 5. Water column depth bin averages of: (A) WR in the surface layer (shaded bars) and the bottom layer (open bars), and (B) GPP (shaded bars), IWR (open bars), and NEM (symbols). Other details as in Fig. 4.

into surface and bottom layer bins, thus omitting mid-depth data for this analysis. Viewed by transect (Fig. 4A), WR rates in the surface layer appeared highest (415 mmol O2 m  3 d  1) along some eastern transects near the Mississippi river mouth, (e.g., transects X and M) and decreasing westward (to about 7 mmol O2 m  3 d  1) through transect H, then increasing slightly at the 3 most westward transects. However, these patterns were not statistically significant, based on an analysis of covariance (ANCOVA) when the confounding effects of water depth and salinity were included as covariates. Spatial patterns in bottom layer WR rates appeared more evenly distributed than surface layer WR rates; peak rates (49 mmol O2 m  3 d  1) were observed on transects M, C, I, and K, and lowest rates (o6 mmol O2 m  3 d  1) were observed on transects B, F, G, and H. Again however, ANCOVA results indicated that these visually apparent spatial patterns were not statistically significant. One highly consistent pattern was that surface layer WR rates were higher than bottom water WR rates. The difference between surface and bottom layer WR rates averaged (7SE) 3.970.39 mmol O2 m  3 d  1, with the surface-bottom differences being significantly larger on transects X, A, and B than the other transects (Po0.01). When viewed by depth bin (Fig. 5A), WR rates were highest in shallow depths, and decreased with increasing water depth for both surface and bottom layers (Po0.01). In the shallowest depth bin ( o10 m), WR rates averaged 412 mmol O2 m  3 d  1 in both surface and bottom layers, whereas at deepest depth bin ( 440 m), WR rates averagedo8 mmol O2 m  3 d  1. As with transect, surface layer WR rates were higher than bottom layer WR rates (Po0.01). The monthly bin averaged WR rates (Fig. 6A) only included 8 months of the year (i.e., no winter data, no July data), so we lack

Fig. 6. Monthly bin averages of: (A) WR in the surface layer (shaded bars) and the bottom layer (open bars), and (B) GPP (shaded bars), IWR (open bars), and NEM (symbols). The year(s) comprising each monthly average is included. Other details as in Fig. 4.

full annual coverage. Furthermore, the cruises were staggered over several years with different flow characteristics, so these month bin averages may not be fully representative of a typical annual cycle. Nevertheless, monthly average surface layer WR rates were consistently highest in the spring and summer months (Mar.–Aug.) and lowest during fall months (Sep.–Nov.). This apparent seasonal progression was not evident in the bottom layer. Again, surface WR rates were consistently higher in the surface layer than in the bottom layer (Po0.01), and the magnitude of the difference appeared to vary seasonally. The surfacebottom difference in WR rates were larger during March to June (range: 4.6–6.7 mmol O2 m  3 d  1) and became progressively smaller in the August to November months (range: 0.1–2.8 mmol O2 m  3 d  1), a trend that was statistically significant (Po0.01). For salinity, we chose bin levels to match those used in plume modeling studies (Breed et al., 2004; Green et al., 2006; Eldridge and Roelke, 2010; Guo et al., 2012); though we used water column average salinity instead of surface-only values (Fig. 7A). WR rates peaked in the mid-salinity bin (18–27) and were lower both lower (0–18) and higher (27–32, 432) salinity bins. The lowest average WR rates were in the highest salinity bin (432). The mid-salinity peak in WR rates was more pronounced in the surface layer than in the bottom layer. To spatially evaluate the susceptibility of LCS waters to O2 depletion (i.e., hypoxia), we calculated the hypothetical time required for WR rates to completely deplete available oxygen in bottom waters (Fig. 8), calculated as the ratio of initial O2 concentration to WR in bottom water samples. The data were

M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

25

76

WR (mmol O2 m-3 d-1)

Surface

20

Bottom

28

15

217

10 183

5 0 350

47

GPP and IWR (mmol m-2 d-1)

17

250 143

Production Respiration NEM

150

134

33

depth. Thus, water column net metabolism was more autotrophic in shallow areas becoming progressively more heterotrophic further offshore (statistically significant in the 440 m depth bin). The uniform integrated productivity across depth zones, originally noted in Lehrter et al. (2009), was somewhat counterintuitive given that nearshore waters typically had high phytoplankton biomass and high volumetric productivity rates relative to offshore waters. However, this pattern reflects the increasing euphotic zone depth as one moves away from shallow turbid waters. Thus, while volumetric productivity was low in offshore waters, this low productivity extended over a larger portion of the water column, resulting in nearly equivalent integrated GPP rates. There was no clear seasonal trends in the monthly averages of GPP and IWR (Fig. 6B), except that both were lowest in October. Net heterotrophy was statistically significant in Mar, May, June, and Oct. Finally, with respect to salinity (Fig. 7B), GPP was higher in low and mid-salinity and declining in the higher salinity zones, whereas IWR declined with increasing salinity. Net autotrophy was significant at mid-salinity (18–27) and net heterotrophy was significant at high salinity (432).

50

4. Discussion -50

4.1. Respiration rates on the LCS and other continental shelf environments

-150 -250 -350 0-18

18-27 27-32 Salinity Bin

>32

Fig. 7. Water column integrated average salinity bin averages of: (A) WR in the surface layer (shaded bars) and the bottom layer (open bars), and (B) GPP (shaded bars), IWR (open bars), and NEM (symbols). Other details as in Fig. 4.

grouped into spring (Mar–May), summer (Jun–Aug), and fall (Sep–Nov) seasons. The resulting contour maps indicated that oxygen depletion times were broadly similar across the seasons, ranging from 10 to 100 d. Spatially, depletion times followed a clear inshore–offshore gradient with shorter times in nearshore waters and longer times in offshore waters. Seasonally, depletion times were shortest during summer, and longer during both spring and fall (grid means: 35, 49, and 45 days, respectively). The time to reach the hypoxic threshold at hypoxia (2 ml l  1) was, of course, shorter, ranging from 6 to 30 days (data not shown). The minimum depletion times ( o10 d) were observed between 901W and 911W (transects A to F), closely coinciding with the region that most frequently experiences summer hypoxia based on historical surveys (e.g., Rabalais et al., 2007). 3.3. Integrated respiration and gross primary production Seasonal and spatial patterns in integrated gross primary production (GPP) and integrated WR rates (IWR) were examined at stations where contemporaneous measurements were made (n¼ 341). With respect to transect (Fig. 4B), both GPP and IWR were highest along eastern transects and generally declined westward. Transects M and B on the eastern LCS appeared were positive (net autotrophic), averaging 145 and 37 mmol m  2 d  1, respectively, though only M was statistically significant. Further west (excluding K), transect means were negative (net heterotrophic) with averages ranging from  17 to  97 mmol m  2 d  1, being statistically significant for transects D, G, and H. With respect to water depth (Fig. 5B), GPP was relatively uniform across all depth zones, whereas IWR increased with increasing

This study provides the most comprehensive empirical description of metabolism on the LCS, and broadly indicates WR rates of about 10 mmol O2 m  3 d  1 in surface waters and about 5 mmol O2 m  3 d  1 in bottom waters. Compared to prior LCS studies (Table 3), this study is of much larger scope, providing measurements over multiple years, over a wider portion of the shelf, and from multiple depths in the water column. Nevertheless, the prior studies did identify key patterns and the overall magnitude in WR rates. For example, several studies found that plume waters had relatively high respiration rates compared to offshore waters (e.g., Amon and Benner, 1998) and that WR rates in surface waters were consistently higher than bottom waters (e.g., Biddanda et al., 1994; Fry and Boyd, 2010). There are few studies of similar scope from other continental shelf environments; the existing studies have reported WR rates of a similar magnitude, and having similar seasonal and spatial patterns. In a global synthesis of marine surface waters, Robinson and Williams (2005) reported WR rates that ranged from 4.6 mmol O2 m  3 d  1 in the nearshore regions (0–20 m depth) to a minimum of  1.2 mmol O2 m  3 d  1 in waters deeper than 80 m. Similarly, several studies from the South Atlantic Bight (Pomeroy et al., 2000; Jiang et al., 2010; Sheldon et al., 2012) reported respiration rates that were lower than the LCS, but having a similar decreasing trend with increasing water depth. Chen et al. (2006) reported WR rates from the East China Sea averaging 9.5 and 3.3 mmol m  3 d  1 for June and August, respectively. They noted a strong coupling between WR rates and phytoplankton, which were both related to seasonal dynamics in nutrient delivery from the Changjiang river. The physical similarities between the East China Sea and the LCS are notable, given that both are low-latitude continental shelf environments dominated by major river systems subject to cultural eutrophication and hypoxia. Based on these comparisons, the overall magnitude and spatial patterns in WR rates we observed were consistent with the literature from both the LCS and other continental shelf environments. 4.2. Coupling between respiration and phytoplankton proxies The relationships among various proxies of heterotrophic (e.g., respiration, bacterioplankton abundance and production) and

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M.C. Murrell et al. / Continental Shelf Research 52 (2013) 27–38

Fig. 8. Shaded contour maps of oxygen depletion time (days) for bottom waters calculated as the ratio of in situ O2 concentration and WR. The data were combined from the 10 cruises into seasonal averages: (A) spring (Mar–May), (B) summer (Jun–Aug), and (C) fall (Sept–Nov). Shown are contours lines for 10, 20, 40, 60, and 80 days.

Table 3 Summary of literature reporting plankton community respiraiton rates (WR) for the Louisiana continental shelf, including means, standard errors (SE), range, and number of observations (n). Water column layers sampled include surface (S), mid-depth (M) and bottom (B). To facilitate comparisons, units were converted to mmol O2 m  3 d  1 when necessary. Also, when necessary, values were estimated from figures in the source reference and standard errors were calculated from respective standard deviations. bd ¼below detection limit; N/A¼ not available.

Months

July, Nov. Feb. Oct. May–Oct. May May, July Mar., Apr., July, Aug. July July Mar., Apr., June, Aug–Nov.

Layers

B S S, S, S S S, S S, S,

M, B M, B

M, B B M, B

WR (mmol O2 m  3 d  1)

Source

Mean

SE

Range

n

1.87 9.23 4.13 0.69 35.9 10.2 15.9 30.2 14.1 8.66

70.22 71.90 71.12 70.09 719.3 N/A 72.82 77.40 72.12 70.24

0.08–6.00 1.47–19.7 1.20–10.8 0.005–4.44 0–41.7 8.2–12.2 0.60–75.0 8.9–75.6 N/A bd–99.3

61 10 2 98 4 2 36 9 165 1289

Turner and Allen, 1982 Chin-Leo and Benner, 1992 Biddanda et al., 1994 Dortch et al., 1994 Pakulski et al., 1995 Amon and Benner 1998 Turner et al., 1998 Pakulski et al., 2000 Fry and Boyd, 2010 This study

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35

Log10WR (mmol O2 m-3 d-1)

GPP slightly more frequently ( 60% of the observations) than the opposite pattern, indicating the prevalence of net water column heterotrophy.

1.5 4.3. Comparison of respiration rates from empirical and model studies

0.5

-0.5 -1.5

Lakes Estuaries Oceans This study

-0.5

0.5

1.5

Log10Chl a (mg m-3)

Log10IWR (mmol m-2 d-1)

3.0

2.0

1.0 Surface Ocean P=R This study

0.0 0.5

1.5

2.5

Log10GPP (mmol m-2 d-1) Fig. 9. (A) Log–log plot of chlorophyll a (Chl-a) and plankton community respiration (WR) in this study. The reduced major axis regression is Log  WR ¼ 0.70  Log  Chl-a þ0.67, r2 ¼ 0.28, n¼1078. Included for comparison are literature consensus regression lines for lakes, oceans and estuaries (del Giorgio and Williams, 2005); (B) Log–log plot of water column integrated primary production (GPP) and plankton respiration (IWR). The reduced major axis regression is Log  IWR¼ 0.82  Log  GPPþ 0.47, r2 ¼ 0.11, n¼ 341. Included for comparison are the P¼ R lines and the literature consensus regression line for surface ocean waters (Robinson and Williams, 2005).

autotrophic (chlorophyll a, primary productivity) metabolism have been widely used to describe the nature and strength of coupling in the underlying metabolic processes across a wide range of aquatic environments (e.g., Cole et al., 1988; del Giorgio and Williams, 2005). We examined the relationship between chl a (a proxy for labile organic matter) and WR rates on the LCS (Fig. 9A), and compared these to consensus relationships for lakes, estuaries and oceans, as synthesized in del Giorgio and Williams (2005). Overall, data for the LCS showed characteristically strong coupling between these independent measures, that was similar to the consensus relationships, with the data cloud appearing to fall in a region intermediate between estuarine and ocean environments. While the strength of the coupling was strongly significant (p 50.001), the regression model explained a relatively small proportion of the variance (r2 ¼0.28), similar to that in literature models for estuarine (r2 ¼0.38) and oceanic (r2 ¼0.27) environments (del Giorgio and Williams, 2005). Similarly, contemporaneous measures of integrated primary production (GPP) and respiration (IWR) suggested coupling between these autotrophic and heterotrophic processes (Fig. 9B). While the data cloud was widely distributed about the 1:1 line, IWR exceeded

Our extensive empirical measurements of water column respiration across the LCS provide a means of evaluating models developed for the LCS that predict the magnitude and spatial and seasonal patterns in respiration rates. Of the numerous LCS modeling studies, we know of only 3 that report respiration rates as part of the model output. First, Bierman et al. (1994) constructed a mass balance box model for phytoplankton, nutrients, and O2, representing the LCS as a series of 21 interconnected segments and calibrated against field data from July 1990. The model predicted a 5-fold longitudinal gradient in bottom water volumetric WR rates, ranging from a low of  4.7 mmol O2 m  3 d  1 near the Mississippi river increasing westward to 22 mmol O2 m  3 d  1 on the western Louisiana shelf (estimated from their Fig. 9). This longitudinal gradient reinforced the view that organic matter produced in Mississippi river plume waters is transported westward and sinks to the bottom, where it contributes to hypoxia formation. Our summer WR rates were of a similar magnitude as Bierman et al. (1994), and showed a subtle longitudinal gradient (perhaps 2-fold), but in the opposite orientation (decreasing westward) as predicted by Bierman et al. (1994). A second model (Justic´ et al., 1996, 1997, 2002, 2003) used a coupled biological–physical oxygen transport scheme to simulate seasonal oxygen dynamics at station C6 on the eastern LCS, a wellstudied site that commonly experiences hypoxia. Using monthly survey data from 1985 to 1993 for calibration, the model produced monthly average respiration rates integrated over the bottom 10 m of the water column, which was the approximate location of the pycnocline. Reported total below pycnocline respiration rates (including sediments) ranged from 0.01 to 33.4 g O2 m  2 month  1 or an equivalent WR of 0.005–3.48 mmol O2 m  3 d  1. Our monthly average bottom water WR rates were several fold higher, ranging from 5.2 to 8.0 mmol O2 m  3 d  1 (Fig. 6A). Including sediment respiration to our WR rates, estimated to be  20% of the below-pycnocline oxygen demand (Murrell and Lehrter, 2011), would make such a comparison between model and measurements diverge further. The reason for such a large discrepancy is currently unclear, but highlights the need for reconciling model and empirical results in order to advance our understanding of oxygen dynamics in the region. A third study used the Streeter–Phelps river model to simulate oxygen dynamics downstream from point sources of organic matter on the LCS (Scavia et al., 2003; Scavia and Donnelly, 2007). This model generated a May–August average belowpycnocline respiration rate (including sediments) equivalent to 1.670.8 mmol O2 m  3 d  1, or about 5-fold lower than our water-only measurements. Similar to the prior example, including sediments would cause the comparisons to further diverge. In summary, models that have predicted respiration rates appear to differ strongly from empirical measurements in magnitude and in seasonal and spatial patterns. While it is difficult to make perfect comparisons between the available models and the measurements reported here, it does provide a new perspective that can help constrain future models of oxygen dynamics for the LCS. 4.4. The case for net heterotrophy on the LCS The net metabolic balance of continental shelf environments is currently debated in the global carbon research community, but heterotrophy has been consistently noted in lower latitudes based

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primarily on air–sea CO2 flux studies (e.g., Borges, 2005; Chen et al., 2006; Jiang et al., 2010; Cai, 2011). Consistent with this view, we observed net heterotrophy in many of the various bin averages, being statistically significant along 3 transects (D, G, and H) in the middle portion of the LCS, at depths 440 m, during Mar., May, June, and October, and in the high salinity waters 432. In contrast, instances of net autotrophy (where GPP exceeded IWR) were relatively rare, being only significant along the M transect nearest the Mississippi river in mid-salinity waters in the river plume. It should be noted that these estimates only included the water column, thus did not include sediment respiration. Similarly comprehensive sediment respiration measurements are not available for the LCS, making it difficult to make a full evaluation. However, in companion studies Lehrter et al., 2012 reported averaged total sediment respiration rates (as DIC fluxes) of 16.571.0 mmol C m  2 d  1 ( 7SE), and Murrell and Lehrter (2011) reported oxygen-based respiration rates of 11.672.2 mmol O2 m  2 d  1. While smaller than typical water column respiration rates (range: 105–263 mmol C m  2 d  1 in Figs. 4–7), accounting for sediment respiration further increases the likelihood that the LCS is heterotrophic. Based on monthly bin averaged data, we estimated that net water column metabolism was 30 mmol C m  2 d  1 from Mar. to Oct. Adding a nominal sediment respiration of 15 mmol C m  2 d  1 yields  45 mmol C m  2 d  1. For sake of this exercise, if we annualize these rates assuming that net metabolism is balanced from Nov. to Feb., then we arrive at  30 mmol C m  2 d  1 or  11 mol C m  2 y  1. While admittedly speculative and poorly constrained, this value is larger than air–water CO2 flux estimates from heterotrophic continental shelves, typically  1 to  3 mol C m  2 y  1 (Borges, 2005). To support the argument that the LCS is net heterotrophic, it is useful to compare the relative magnitudes of net heterotrophy estimated above ( 11 mol C m  2 y  1) to first-order estimates of allochthonous organic carbon inputs to the LCS. Two major sources of allochthonous material were considered, namely terrestrial organic matter delivered in river water, and marine-derived organic matter from eutrophic nearshore waters. First, the Mississippi and Atchafalaya rivers deliver an enormous quantity of organic carbon (dissolved and particulate) to the LCS, on the order of 4.8  1011 mol C y  1 (Trefry et al., 1994). Granted, only a fraction of this organic matter is likely delivered to the shelf, principally because about half of the Mississippi river flow (and accompanying DOC) is advected off of the shelf (Dinnel and Wiseman, 1986), and a portion of the riverine POC is deposited and processed outside of the domain (Xu et al., 2011). Thus, if only half of the riverine OC is respired on the shelf (assuming 40,000 km2), this would amount to 6 mol C m  2 y  1 or 55% of the organic C deficit indicated above. Second, the shallow inshore waters along the coastline likely represent a source of organic matter that episodically may be delivered to the LCS. These highly productive waters, include the plume waters entrained in the Louisiana Coastal Current, and the inland bays dominated by Atchafalaya river flow (e.g., Fourleague, Atchafalaya, West Cote Blanche, and Vermilion Bays), which collectively comprise  6000 km2. While primary productivity data are sparse, Madden et al. (1988) reported net phytoplankton productivity of 519 g C m  2 y  1 for lower Fourleague Bay. If we assume this magnitude of productivity is representative of inshore waters, then this amounts to an additional 2.6  1011 mol C y  1, or 6.5 mol C m  2 y  1 available for transport onto the shelf. While some fraction of the inshore productivity is likely respired in situ, periodic atmospheric cold fronts during winter and spring can cause large-scale transport of organic matter from the inland waters to offshore waters of the LCS (Perez et al., 2000, 2003). Thus, inshore productivity could supply up to 59% of the organic C deficit estimated from our shelf-wide estimate above. Unlike river-

derived organic C, this phytoplankton-derived organic matter is very labile, thus is likely respired rapidly. Thus, phytoplankton from nearshore waters that is periodically exported to the shelf can be a potentially important source of organic matter supplementing LCS metabolism. 4.5. Sensitivity of results to model assumptions It is important to consider that our estimates of net metabolism are indirect, relying on assumptions to translate rate measurements from discrete water samples into water column integrated estimates. Perhaps the two most important assumptions are those used to convert net to gross primary production and the choice of RQ for converting WR rates into carbon equivalents. First, to calculate gross primary production, we assumed that phytoplankton respiration was a fixed 10% of light-saturated photosynthesis. In reality, this is not a constant proportion, rather it likely varies with environmental conditions (e.g., temperature, irradiance, mixing characteristics) and with taxonomic composition of the phytoplankton community (Geider and Osborne, 1989). Not surprisingly, net metabolism calculations will be sensitive to the value used. For example, increasing phytoplankton respiration from 10 to 15% of light-saturated photosynthesis results increased estimates for both gross primary production and net metabolism. In the above annualized example, carrying this single change through the scale calculation causes net metabolism estimate to increase from  11 to  6 mol C m  2 y  1. Second, we assumed an RQ¼1 (CO2 evolved per O2 consumed) to convert respiration rates to carbon equivalents, yet this ratio will vary depending on the organic matter source being oxidized. While RQ values can vary from 0.5 to 1.3, the range should be much narrower (0.9 to 1.1) if the organic matter source is predominantly plankton. As with phytoplankton respiration, the choice of RQ directly affects net metabolism estimates. For example, changing RQ from 1.0 to 1.1 would decrease annualized net metabolism estimate from  11 to  15 mol C m  2 y  1. Thus, better and more site-specific estimates of both phytoplankton respiration and RQ would improve net metabolism estimates. Nevertheless, using nominal conversion factors, net heterotrophy is commonly indicated on the LCS. 4.6. Concluding remarks In summary, this study provides one of the largest and most comprehensive datasets of plankton respiration from a continental shelf environment. The data show coherent spatial and seasonal patterns that appear consistent with the relatively sparse data available for continental shelves in general and the LCS in particular. The spatial and seasonal patterns in oxygen turnover rates were consistent with historical patterns of hypoxia. While our results appeared similar in several respects to prior LCS empirical studies, they differed significantly from model studies that estimated respiration rates for the LCS. As such, this large empirical dataset should help refine and constrain future models of oxygen dynamics in the region. We found consistent evidence for heterotrophy on the LCS, implying that organic matter from outside the system was subsidizing metabolism. We offer simple scale arguments to demonstrate how riverine and marine-derived organic matter are potentially significant sources of this allochthonous organic matter. Clearly, further study is needed to develop a comprehensive picture of the key carbon sources and sinks on the LCS.

Acknowledgements This study was only possible from contributions from many individuals. Programmatic leadership was provided by R. Greene. For shipboard and laboratory assistance, we thank L. Anderson, J.

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Aukamp, D. Beddick, J. Campbell, G. Craven, F. Genthner, B. Jarvis, J. Kurtz, and B. Quarles, and D. Yates. Comments from J. Caffrey, E. Smith and 3 anonymous reviewers helped improve the manuscript. Financial support for ship time was provided by the US EPA’s Office of Water and Gulf of Mexico Program Office. We thank the crews of the Ocean Survey Vessel (OSV) Peter W. Anderson (decommissioned), the OSV Bold, and the R/V Longhorn. This study was funded by the US EPA, but the contents are solely the views of the authors. Use of trade names does not constitute endorsement by the US EPA. References Amon, R.M.W., Benner, R., 1998. Seasonal patterns of bacterial abundance and production in the Mississippi river plume and their importance for the fate of enhanced primary production. Microbial Ecology 35, 289–300. Bevington, P.R., 1969. Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, Inc, New York 336 p. 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