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ARTICLE IN PRESS Continental Shelf Research 28 (2008) 1527– 1537 Contents lists available at ScienceDirect Continental Shelf Research journal homepage: www.elsevier.com/locate/csr Comparison of hypoxia among four river-dominated ocean margins: The Changjiang (Yangtze), Mississippi, Pearl, and Rhône rivers C. Rabouille a,, D.J. Conley b, M.H. Dai c, W.-J. Cai d, C.T.A. Chen e, B. Lansard a, R. Green f,1, K. Yin g,i, P.J. Harrison g, M. Dagg f, B. McKee h a Laboratoire des Sciences du Climat et de l’Environnement, UMR CEA-CNRS-UVSQ and IPSL, Av. de la Terrasse, 91198 Gif sur Yvette, France GeoBiosphere Science Centre, Department of Geology, Lund University, Sölvegatan 12, SE-223 62 Lund, Sweden c State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, China d Department of Marine Sciences, The University of Georgia, Athens, Georgia 30602, USA e Institute of Marine Geology and Chemistry, National Sun Yat-sen University, Kaohsiung 80424, Taiwan f Louisiana Universities Marine Consortium, 8124 Highway 56, Chauvin, LA 70344, USA g Atmospheric, Marine and Coastal Environment Program, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China h Department of Marine Sciences, University of North Carolina, Chapel Hill, NC 25599, USA i Australian Rivers Institute, Griffith University (Nathan Campus), Brisbane, Qld. 4111, Australia b a r t i c l e in fo abstract Available online 13 March 2008 We examined the occurrence of seasonal hypoxia (O2o2 mg l1) in the bottom waters of four riverdominated ocean margins (off the Changjiang, Mississippi, Pearl and Rhône Rivers) and compared the processes leading to the depletion of oxygen. Consumption of oxygen in bottom waters is linked to biological oxygen demand fueled by organic matter from primary production in the nutrient-rich river plume and perhaps terrigenous inputs. Hypoxia occurs when this consumption exceeds replenishment by diffusion, turbulent mixing or lateral advection of oxygenated water. The margins off the Mississippi and Changjiang are affected the most by summer hypoxia, while the margins off the Rhône and the Pearl rivers systems are less affected, although nutrient concentrations in the river water are very similar in the four systems. Spring and summer primary production is high overall for the shelves adjacent to the Mississippi, Changjiang and Pearl (1–10 g C m2 d1), and lower off the Rhône River (o1 g C m2 d1), which could be one of the reasons of the absence of hypoxia on the Rhône shelf. The residence time of the bottom water is also related to the occurrence of hypoxia, with the Mississippi margin showing a long residence time and frequent occurrences of hypoxia during summer over very large spatial scales, whereas the East China Sea (ECS)/Changjiang displays hypoxia less regularly due to a shorter residence time of the bottom water. Physical stratification plays an important role with both the Changjiang and Mississippi shelf showing strong thermohaline stratification during summer over extended periods of time, whereas summer stratification is less prominent for the Pearl and Rhône partly due to the wind effect on mixing. The shape of the shelf is the last important factor since hypoxia occurs at intermediate depths (between 5 and 50 m) on broad shelves (Gulf of Mexico and ECS). Shallow estuaries with low residence time such as the Pearl River estuary during the summer wet season when mixing and flushing are dominant features, or deeper shelves, such as the Gulf of Lion off the Rhône show little or no hypoxia. & 2008 Elsevier Ltd. All rights reserved. Keyword: Oxygen Hypoxia Carbon cycle Coastal oceanography Estuaries River plumes Nutrients Continental shelves 1. Introduction Regional index terms: China, Changjiang (Yangtze River), East China Sea; USA, Mississippi River, Gulf of Mexico; China, Pearl River, South China Sea; France, Rhône River, Gulf of Lion. Corresponding author. E-mail addresses: [email protected] (C. Rabouille), [email protected] (D.J. Conley), [email protected] (M.H. Dai), [email protected] (C.T.A. Chen), [email protected] (R. Green), k.yin@griffith.edu.au (K. Yin), [email protected] (P.J. Harrison), [email protected] (M. Dagg), [email protected] (B. McKee). 1 Current address: Ocean Optics Section, Naval Research Laboratory, Stennis Space Center, MS 39529, USA. 0278-4343/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.csr.2008.01.020 Eutrophication and its consequences are an increasing threat to coastal ecosystems through harmful algal blooms, alteration of plankton community structure, and hypoxia in bottom waters (Cloern, 2001). These impacts are believed to be associated with high nutrient loads delivered by rivers to estuaries and ultimately to the coastal waters. Although the presence of hypoxia and anoxia has existed through geologic time, the occurrence in coastal waters has been accelerated by human activities (Diaz, 2001). ARTICLE IN PRESS 1528 C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 Large rivers exert a strong influence on the continental shelves over which they discharge, forming stratified and turbid plumes in their estuaries and outside on the shelves throughout the year and especially during the high discharge periods (Dagg et al., 2004; Mckee et al., 2004; Dai et al., this issue). In addition, elevated nutrient concentrations in river waters often trigger high primary production and algal blooms in the river plume, and the adjacent shelf water (Lohrenz et al., 1997; Dagg and Breed, 2003). A portion of the organic matter produced in the plume, along with terrestrial inputs, settles to the seafloor where it is decomposed by benthic fauna and bacteria using oxygen. When vertical exchange of the water is limited (i.e. stratification), the oxidation of organic matter may reduce oxygen below 2 mg l1 (or 62.5 mmol l1) producing a state of hypoxia (Rabalais et al., 2002) where benthic fauna become stressed or die due to the lack of oxygen (Diaz and Rosenberg, 1995). Hypoxia may ultimately lead to anoxia where oxygen completely disappears and sulfide may diffuse from the sediment to the bottom water, both causing mass mortality of organisms (Smetacek et al., 1991). Several estuaries and continental shelves of the world coastal ocean undergo severe hypoxia including the Chesapeake Bay, USA (Hagy et al., 2005), the Danish Straits (Conley et al., 2007), and the Mississippi River outlet in the northern Gulf of Mexico which is one of the largest areas of the world with seasonal hypoxia (Rabalais et al., 2002). Other estuaries or river-dominated margins such as the Changjiang in China (Zhou and Shen, this issue; Wei et al., 2007) and the St. Lawrence River in Canada (Gilbert et al., 2005), exhibit hypoxia in the inner or outer part of their estuaries. The decrease of oxygen from saturation (250–300 mmoll1) to hypoxic levels occurs when both thermal and haline stratification of the water due to freshwater discharge and summer warming, nutrient utilization by phytoplankton, and subsequent settling of phytoplankton to bottom waters, occur in the right sequence. Yet, some shelves adjacent to large rivers do not exhibit hypoxia and large variations in the volume of hypoxic waters are known to occur within hypoxic systems (Hetland and DiMarco, 2007) indicating that there are complex interactions between physical, chemical, and biological processes causing and maintaining hypoxia in river-dominated ocean margins. In this paper, we compare the physical, chemical, and biological processes leading to the formation, occurrence, and intensity of hypoxia in four river-dominated ocean margins which receive large amounts of river-derived organic loading and dissolved nutrients: the Changjiang (Yangtze River), Mississippi, Pearl (or Zhujiang), and Rhône Rivers. These margins are all impacted by their river inputs, but only some of these margins exhibit hypoxia. We will compare the occurrence of hypoxia in these four estuaries/shelves with their nutrient/organic inputs and their physical settings (tides, margin shape, shelf currents, water residence times, and wind regimes) in order to identify general principles about the development and maintenance of coastal hypoxia. 2. Locations and characteristics of the four estuaries/shelves 2.1. Geographical location and discharge All four river systems are located in the northern hemisphere and three of them discharge at latitudes between 201N and 321N: the Pearl, Changjiang, and Mississippi Rivers (Table 1). The Pearl and Changjiang watersheds are dominated by the monsoon but the Mississippi watersheds is mostly temperate. Only the Rhône River is located north of 431N and is thus a completely temperate river system (Fig. 1). On a global basis, the Mississippi and the Changjiang are large rivers, while the Pearl is somewhat intermediate and the Rhône River is significantly smaller in discharge (Table 1). The seasonality of the discharge is similar for the Pearl and Changjiang with high flows in summer associated with the monsoon rain, whereas the Mississippi and Rhône show low water discharge in summer and higher water fluxes in autumn and spring, due to autumn rain and spring snowmelt (Fig. 2). The Changjiang is the longest river in China (6200 km) and drains a large portion of central continental China (Table 1). It discharges into the East China Sea (ECS) mainly through its south branch which discharges more than 95% of the runoff (Cai et al., this issue). The annual freshwater discharge of the Changjiang ranked fifth in the world and fourth for sediment discharge (Milliman and Meade, 1983; Meade, 1996) before the Three Gorges Dam was built. This discharge is highly seasonal with 75% of the river runoff occurring during the flood/rainy season between May and October. According to Yang et al. (2007), the building of the Three Gorges Dam has resulted in a decrease (by 30%) in sediment discharge. The Mississippi–Atchafalaya River basin drains approximately 41% of the USA and carries approximately 65% of all the suspended solids and dissolved solutes that enter the ocean from the USA. It effectively injects these materials onto the continental shelf as two point sources in the northern Gulf of Mexico. The Mississippi–Atchafalaya River system has the third largest drainage basin among the world major rivers (Table 1; Milliman and Meade, 1983; Meade, 1996). This river system also ranks seventh in freshwater discharge and fifth in sediment discharge. About two-thirds of the total flow passes through the birdfoot delta of the Mississippi River and discharges into the outer shelf region, with the remainder flowing into Atchafalaya Bay before entering the Gulf of Mexico on the coast (Wiseman and Garvine, 1995). The Pearl River is the 13th largest river in the world in terms of freshwater discharge and has an annual sediment delivery of 80 Mt (Table 1; Zhao, 1990). It discharges into the sub-tropical, oligotrophic South China Sea (SCS). Together with the Mekong River, they provide the largest freshwater input to the SCS, which is the largest marginal sea in the north Pacific. The Pearl River estuary is a complex estuarine system (Cai et al., 2004; Harrison et al., this issue) which discharges into the SCS through three subestuaries, Lingdingyang, Maodaomen, and Huangmaohai via eight main outlets, or distributaries. It is fed mainly by three river tributaries, namely the Xi-jiang (West River), the Bei-jiang (North Table 1 Major characteristics of the four river systems Changjiang Mississippi Pearl Rhône Length (km) Latitude of river mouth (1N) Drainage basin (103 km2) Freshwater discharge (109 m3 yr1) Sediment discharge (Mt yr1) 6200 6300 2200 800 311300 N 291000 N 221300 N 421500 N 1800 3210 450 100 924 530 330 53 486 210 80 10 ARTICLE IN PRESS C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 1529 Fig. 1. World map with the location of the four river-dominated ocean margins systems presented in this study. Monthly discharge (m3/s) 60000 Table 2 Annual nutrient and carbon discharge from the four river systems Pearl River Changjiang River Mississippi River Rhone River *5 50000 Freshwater discharge (109 m3 yr1) 40000 Nutrient Input (109 mol yr1) DIN 30000 a Changjiang Mississippib Pearlc Rhôned 20000 924 530 330 53 a 116 68 28 8.8 DIP a 0.3 1.3 0.3 0.08 DSi 100 72 46 4.8 a DOC POC – 150 – 11 – 317 – 16 10000 a Shen et al. (2006). Goolsby et al. (1999). c Cai et al. (2004). d De Madron et al. (2003). b 0 0 2 4 6 Month 8 10 12 Fig. 2. Monthly discharge of the four river systems. Rhône River discharge is multiplied by 5 to match the scale. 2.2. Nutrient discharge from the rivers River), and the Dong-jiang (East River). The West River has the greatest freshwater discharge (78% of the total discharge). The Rhône River is located in the south of France and is the largest freshwater input to the Mediterranean Sea since the damming of the Nile River in Assouan. It receives water from a drainage basin which spans temperate and Mediterranean climatic regions (Table 1; Pont et al., 2002). The Rhône delta is divided into two outlets, the Petit Rhône and the Grand Rhône, corresponding to 20% and 80% of the water flow, respectively. Discharge is characterized by the occurrence of autumn and winter floods which may be 20 times higher than the remainder of the year and reach 410,000 m3 s1. Inputs from these episodic floods are not well quantified; giving rise to uncertainties on the particle discharge at the mouth of the river (1075 Mt y1). The amount of dissolved inorganic nitrogen (DIN) discharged by the four rivers is clearly linked to the water discharge volume (Table 2). The Changjiang has the largest input of DIN and the Mississippi, Pearl, and Rhône Rivers have lower values. In these human impacted systems, a large fraction of the nitrogen inputs are due to agricultural practices as well as sewage and industrial sources. All four basins are dominated by agriculture strongly affecting the relationship between freshwater and nutrient discharge. This is reflected in the high DIN concentrations of the rivers: 20–200 mM for the Mississippi (Dagg et al., 2004), 75–100 mM for the Pearl (Cai et al., 2004), and 60–160 mM in the Changjiang (Shen, 2004) and the Rhône (De Madron et al., 2003). Dissolved inorganic phosphorus (DIP) fluxes are linked to the geology of the river watershed and its weathering in addition to ARTICLE IN PRESS 1530 C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 the fertilizer input. Therefore, the load of the rivers is not strictly related to water discharge and DIP loadings for Changjiang and Pearl are similar, although the Changjiang discharge is three times larger (Table 2). The DIP concentrations are low in all seasons in the Pearl (seldom 4 1 mM), while the other three rivers have a considerable range and larger average concentrations. DSi concentrations range from 90 mM in the Rhone to 140 mM in the Pearl and are below the world average DSi concentration of 150 mM (Treguer et al., 1995). DOC and particulate organic carbon (POC) inputs have been reported only for the Rhône (Sempéré et al., 2000) and Mississippi (Trefry et al., 1994). 2.3. Dynamics of shelf bottom waters Tidal range is a key determining characteristic for the development of deltas (Syvitski and Saito, 2007) because it greatly affects the rate of exchange with the coastal sea. The tidal range for the four deltas/estuaries is mostly microtidal (Table 3) with the exception of the Changjiang, which slightly exceeds 2 m and is mesotidal. The Pearl tidal range is 0.86–1.89 m at the main outlet. Among the four systems considered in this paper, building of the Rhône and Pearl deltas is significantly affected by waves, whereas the Changjiang and Mississippi deltas are mostly affected by river sediment discharge (Syvitski and Saito, 2007). Thermal stratification is strong for the Mississippi, Pearl, and Changjiang margins during summer (Table 3). While discharge is low, there is sufficient freshwater inflow from the Mississippi, coupled to calm winds, to further strengthen the pycnocline and Table 3 Tidal range, summer stratification, and bottom current speed Changjianga Mississippib Pearlc Rhôned Average tidal range (m) Stratification Bottom current (cm s1) Wind speed in summer (m s1) 2.5 1 1.4 0.4 Strong Strong Strong Medium 25–30 2–5 25–50 10–15 4 2.5 10 a Zhu et al. (2004). Zavala-Hidalgo et al. (2003); Wiseman et al. (2003). c Yin et al. (2000). d Lansard, (2004). b support the spreading of the plume. Freshwater discharge peaks in summer for the Changjiang and Pearl and also promotes density stratification. In the ECS close to the Changjiang mouth, the interaction of freshwater discharge and the Taiwan Warm Current (TWC) with high salinity and high temperature water at depths near 30 m contributes to stratification (Li et al., 2002; Wei et al., 2007; Zhu et al., 2004). In the SCS near the Pearl River mouth, the water is stratified during spring–summer when the estuarine plume forms. There is little or no stratification in winter due to wind mixing. Average winter wind speeds (10 m s1) are four times higher than summer (2.5 m s1; Yin, 2002). Stratification is less established in summer for the Rhône margin, because frequent high winds disrupt the density structure (Estournel et al., 2001). Summer bottom currents range from weak (0.5–5 cm s1) to strong (50 cm s1) among the four margins (Table 3). Summer surface currents are 5–10 cm s1 beyond the immediate plume of the Mississippi (Zavala-Hidalgo et al., 2003) and bottom currents at 20 m in an area of frequent hypoxia are lower (0.5–2 cm s1; Wiseman et al., 2003). The current reversal occurring at the end of spring creates a temporary low in the transport rate in June, July and August (Smith and Jacobs, 2005). Due to the TWC water, speeds off the Changjiang are about 30 cm s1 throughout the year (Li et al., 2002; Zhu et al., 2004). Bottom currents on the Rhône prodelta show intermediate speeds of 10–15 cm s1 during late spring at 16 m depth (Lansard, 2004) which are consistent with current velocities measured at the shelf edge at 240 m during summer (5–10 cm s1; Flexas et al., 2002). Current speeds are the highest in the Pearl River estuary reaching values of 50 cm s1, which results in a residence time (volume of the estuary divided by the freshwater flow) of days during the wet season (March– October; Yin et al., 2004a), and a couple of weeks in the dry season (Dai, unpublished data). For the Rhône, Changjiang, and Mississippi margins, residence time of the bottom water can be calculated using current velocities and an estimation of the extent of the zone of higher oxygen demand due to river inputs (Fig. 3). The size of this zone was estimated from the zone of river-plume primary production (Table 4) because primary production is the main source of organic matter for fueling hypoxia (Green et al., 2006). The residence time of the water is calculated as the ratio between the volume of water in this box and the lateral flux of water through the box: tres ¼ V hypoxic =F water , Surface water River input Depth = 0 m Upper shelf Depth = 30-50 m bottomwater water(pot. (pot. hypoxic) bottom hypoxic) sion xten L : E system e of th S: surface S: surfacearea area nt ω ore Lower shelf re cur gsh n Alo Depth = 100 m Fig. 3. Schematic diagram of alongshore circulation in bottom waters. The upper box represents surface water which receives the river input while the lower box represents bottom waters which may become hypoxic. L is the alongshore extension of the system, S is the cross-section of the system through which the alongshore current runs and o is the speed of the alongshore current. ARTICLE IN PRESS C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 0 Table 4 Current speed in intermediate and deep waters near the river mouths, the extension of the mixing system, and the calculated residence time 10 River 30 Pearl Rhône a Taiwan warm current 30 Louisiana bottom current 2–5b,c Estuarine mixing Lingdingyan Ligurian bottom current (20–40 m) 10e Extension of the system—L (km) 300 400 Residence time tres (d) 11 95 d 50 3–5 50 6 Pearl River 20 Depth (m) Changjiang Mississippi Alongshore current speed o (cm s1) Rhône shelf 40 50 60 Rhône prodelta 70 80 0 V hypoxic ¼ Sbox L and F water ¼ Sbox o, where Sbox being the lateral surface area of the box considered, o the current speed (cm s1), and L the extension of the system alongshore (km). The residence time can thus be expressed by tres ¼ L=o. Residence times (Table 4) show a large range from 6 to 95 days. The largest values occur on the Mississippi shelf due to a combination of low currents and a large extent of the system. The Changjiang is intermediate with a value of 11 days and Rhône and Pearl are the lowest. 2.4. Bathymetry of the shelf close to the river mouth Mississippi, Changjiang, and Rhone freshwater plumes extend far onto the continental shelf and mix with seawater of the continental margin. The Pearl River has a seasonal plume that stretches onto the shelf only during high discharge (Yin et al., 2001), but is otherwise a classic estuarine mixing zone. A broad continental shelf characterizes the Pearl, Changjiang, and Mississippi (Fig. 4), while the Rhône shelf reaches depths 4100 m within 40 km of the river mouth. The subaqueous deltas of the Rhône and Mississippi are prograding onto the shelf, which results in steep slopes to depths of 100 m within 10–20 km of the river mouths (Fig. 4). Mississippi shelf 100 20 40 60 80 100 Distance (km) b where tres is the residence time of the bottom water in the hypoxic part of the shelf with regards to lateral current, Vhypoxic is the volume of potential hypoxic waters, and Fwater the flux of water through that volume. If the geometry is rectangular, this problem can be simplified since Changjiang Mississippi delta 90 a Zhu et al. (2004). Zavala-Hidalgo et al. (2003). c Wiseman et al. (2003). d Yin et al. (2000). e Lansard, (2004); Flexas et al. (2002). 1531 Fig. 4. Bathymetry of the four coastal systems at the river outlet. The four thick lines represent the very shallow estuary of the Pearl River, the shelf of the Changjiang, the Louisiana shelf west of the Mississippi and the shelf west of the Rhône. Thinner lines (Rhône and Mississippi) display bathymetric features at the river mouth, which are characterized by prodeltas and steep slopes. concentration measured in the core of this hypoxic region was lower in 1999 (Li et al., 2002) than in the 1980s, suggesting that summer hypoxia has increased over time. Recent studies (Chen et al., 2005; Wei et al., 2007) suggested that the spreading of the summer hypoxic zone continued in 2003 (20,000 km2 with o3 mg l1 of oxygen). These studies identified August as the maximum hypoxia period. 3.2. Mississippi The shelf region of the northern Gulf of Mexico that is impacted by the Mississippi and Atchafalaya River systems is the best documented example of hypoxia (Rabalais and Turner, 2001; Rabalais et al., 2002; Dagg et al., 2007). Since 1993, an extensive zone of bottom water hypoxia, typically 415,000 km2, develops during most years (Rabalais et al., 2002). In the northern Gulf of Mexico, hypoxia is seasonal. It starts in late spring and reaches its maximum in late July before fall wind mixing and destratification. Hypoxia occurs in shallow bottom waters (5–40 m) along the coast of Louisiana in regions affected by nutrient inputs from the Mississippi/Atchafalaya River discharge. The oxygen concentration in bottom waters in the center of this hypoxic zone is frequently o1 mg l1 of oxygen (or 31 mmol l1). Generally, there is a strong correlation between the volume of river discharge in spring and summer and the extent of hypoxic waters. During two severe droughts of the Mississippi River in 1988 and 2000, the area of hypoxic bottom water was o5000 km2 (Rabalais et al., 2002; Rabalais and Turner, 2006). In contrast, a much larger hypoxic zone occurred from 1993 to 1997 (415,000 km2), and in 1999 and 2001 when it was 420,000 km2. 3.3. Pearl River 3. Occurrence of hypoxia 3.1. Changjiang Early hydrological surveys off the Changjiang River in summer reported the occurrence of hypoxic waters about 100 km from the river mouth along 1231E at 35 m depth with oxygen concentrations of 1.5–2 mg l1 (Tian et al., 1993). Subsequent surveys identified a zone of low oxygen concentration during the summer (o 3 mg l1) extending over 13,000 km2 with a thickness of 20 m at a depth between 30 and 50 m (Li et al., 2002). The oxygen Hypoxic conditions rarely occur in the lower Pearl River estuary or on the shelf (Yin et al., 2004a). In the summer of 1999 (high river flow), a survey of the estuary showed oxygendepleted waters (around 3–4 mg l1) occurring in several areas of the estuary, but hypoxic waters (o2 mg l1) occurred only around the turbidity maximum at one station (Yin et al., 2004a). A monthly, 10-year (1990–1999) time series around Hong Kong Island (in the eastern estuary and the nearby shelf) also showed low oxygen waters (o3 mg l1), but no hypoxia in the bottom waters (Yin et al., 2004a). ARTICLE IN PRESS 1532 C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 3.4. Rhône River On the continental shelf near the Rhône, near saturation values of oxygen in bottom waters have been reported throughout the year (Denis and Grenz, 2003). In the same area, the data sets for the summer of 2005 and 2006 showed oxygenated water down to 1 m above the seabed (Lansard, pers. comm.). In August 2006, oxygen contents in the Bay of Beauduc located west of the Rhône were near-saturation under windy conditions (Lansard, pers. comm.). Hence, the continental shelf near the Rhône River does not appear to exhibit significant hypoxia. 4. Discussion The occurrence of hypoxic conditions in coastal regions connected to large rivers is due to the interplay between water column production, which supplies organic matter to bottom water and sediment thereby generating oxygen consumption, and physical forcings (stratification, the circulation pattern in the region and residence time of the water in the mixing zone) which limit oxygenation of bottom waters. In spite of large inputs of organic matter to the bottom, the interplay between the physical and biogeochemical forcings for each margin may or may not lead to hypoxia as exemplified by the Changjiang and Mississippi margins in which hypoxia occurs, and the Pearl and Rhône margins where hypoxia is absent. In this section, we draw a comparison of the physical and biogeochemical factors between the four river/margin systems. 4.1. Physical forcings Various physical factors, including the physiography of the margin, water residence time on the shelf, summer stratification and its relation to the wind regime and currents, and tidal magnitude influence the occurrence and intensity of hypoxia. Hypoxia of the coastal shelf near river mouths occurs when oxygen consumption from the decomposition of organic inputs to the bottom waters exceeds the replenishment of oxygen in the bottom waters. Thus, conditions affecting the rate of oxygen replenishment to sub-pycnocline waters by either horizontal advection of water through circulation on the shelf (water residence time, shape of the margin), turbulent vertical mixing by surface cooling and wind/tidal mixing or diffusion across the pycnocline (thermal stratification, tidal regime) are key to determining the development, duration, and extent of bottom water hypoxia (Rowe, 2001). 4.1.1. Shape of the margin The different shapes of the continental shelves near the four rivers influence the occurrence of hypoxia. Among the four systems, shallow (30–50 m) and broad shelves such as Mississippi and Changjiang are linked to the occurrence of hypoxia. Shallow shelves are more subject to summer warming and stronger stratification. They may also experience more intense pelagic– benthic coupling and higher deposition of labile organic matter to the sediments which enhance the local sediment oxygen demand. On the contrary, very shallow depths (5–20 m) such as the Pearl River estuary can facilitate wind-driven vertical mixing of the surface and bottom waters, thereby tending to reduce hypoxia. In contrast, the Rhône shelf which is over 100 m deep, displays no hypoxia. Another feature, which may influence the development or intensity of hypoxia, is the existence of a prodelta (as in the Mississippi and Rhône), which carries water, nutrients, and particles beyond the coastal and shallow shelf. In the current physical configuration of an intensively leveed Mississippi River, it appears that direct sedimentation of terrestrial organic matter from this plume has a relatively small contribution to the development of hypoxia on the shelf (Green et al., 2006), because most of this material is deposited and buried (around 60%) on the deeper shelf adjacent to the river (Corbett et al., 2004, 2006). Rather, hypoxia may be related to the recycled nutrients from the plume that are transported over the broad shallow shelf to the west (Green et al., 2006), or to nutrients discharged by the Atchafalaya at the coast (Green et al., 2006), and supplemented by organic matter inputs from coastal bays and marshes (Dagg et al., 2008). Physical conditions contributing to the transport of Mississippi River water from its discharge site near the shelf break to the coastal region are key factors for hypoxia development. In the case of the Rhône prodelta, the main plume is diverted to the south-west over the deeper shelf and rarely penetrates into a shallower coastal bay, thus preventing its contribution to hypoxia. 4.1.2. Residence time of the bottom water Residence time of bottom waters is a very important factor for hypoxia development, because it directly affects the duration of oxygen consumption during organic matter decomposition and thus the degree of O2 depletion. A long residence time allows complete decomposition of organic matter and large oxygen consumption. Residence time of bottom waters is controlled by horizontal advection of the water under the influence of intermediate and bottom shelf currents. The results from Table 4 show that hypoxia is related to the residence time. The Mississippi system, with the longest bottom water residence time, shows the strongest and largest hypoxia, while the Rhône with a short residence time and the Pearl inside the lower estuary displays no hypoxia. In the ECS/Changjiang zone, hypoxia is less recurrent and temporally shorter which may be partly related to the lower residence time of its bottom water. 4.1.3. Tidal regime, summer stratification Tidal mixing of water can disrupt density stratification which promotes the isolation of bottom water from the atmosphere and the subsequent occurrence of hypoxia (Wiseman et al., 1997). The tidal regime of the four estuaries varies from microtidal (Rhône, Mississippi, about 2 m for the Pearl Rivers) to meso-tidal for the Changjiang (Table 3). There is no correlation between the tidal regime and the occurrence of hypoxia since the Mississippi and the Changjiang margins are at the lower and higher ends of the tidal range yet both undergo seasonal hypoxia. The tidal range in the four systems examined is rather narrow and tidal mixing may not be significant especially for waters at 30–50 m, which are hypoxic during summer. The strength of summer stratification is another variable which may promote hypoxia since it restricts oxygenation of the water by limiting exchanges between the bottom water and the atmosphere. For the Mississippi shelf, a correlation between summer stratification and hypoxia has been proposed (Wiseman et al., 1997; Rowe and Chapman, 2002). Stratification of the Mississippi is shown on Fig. 5. A large decrease in temperature and an increase in salinity of the bottom waters produce high density bottom waters and strong stratification in August. A higher surface temperature is due to heat exchange with the atmosphere and a lower surface salinity is related to the input of freshwater from the river in the Louisiana current. If wind and tidal mixing are low, then hypoxia can occur over a large area. A similar feature occurs in the Changjiang where permanent salinity stratification combines with thermal stratification in late ARTICLE IN PRESS Depth (m) C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 0 0 0 5 5 5 10 10 10 15 15 15 20 20 20 25 25 25 30 30 24 26 30 28 32 34 36 38 1533 30 22 26 24 28 Temperature (°C) Salinity (ppt) 30 32 1.5 2.0 2.5 3.0 3.5 4.0 4.5 Oxygen (mg l-1) Fig. 5. Typical profiles of T, S, and oxygen during hypoxic conditions in the Mississippi system showing strong thermohaline stratification (August 12, 2004, at 28132.860 N, 90154.620 W; M. Dagg unpublished). Table 5 Average summer nutrient concentrations (mM) in four rivers and the nutrient atomic ratio (see reference in the conclusions table) River DIN conc DIP conc DSi conc PIP conc DIN/DIP DIN/TP DIN/DSI Changjiang 125 Mississippi 128 Pearl 85 Rhône 118 0.3 2.5 1 1.2 110 136 140 71 5.8 2.1 417 51 85 98 15 36 1.13 0.9 0.6 1.7 summer (Li et al., 2002). The degree of stratification correlates well with Chl-a concentration and hypoxia occurrence in late summer at the Changjiang mouth (Wei et al., 2007), despite the strong current transporting water from the south in the ECS. The TWC which spreads at intermediate depths further limits oxygen exchange with the surface waters (Li et al., 2002; Zhu et al., 2004). These observations on the Mississippi and Changjiang where hypoxia is recurrent suggest that stratification plays a key role in hypoxia development. Indeed, oxygen depletion is very sensitive to cross-pycnocline exchange (Rowe, 2001) and O2 replenishment, either vertically through the pycnocline or laterally, must be properly quantified. The stratification situation is completely different for the Pearl River for which the highest discharge occurs during summer (July) together with warmest water temperatures. Stratification during the summer cannot develop over long periods because of short water residence time (3–5 days; Yin et al., 2000), monsoon winds and occasional typhoons (Yin, 2002, 2003; Yin et al., 2004c; Harrison et al., this issue) which contribute to the mixing of the estuary. For the Rhône, the occurrence in summer of strong northwestern winds (410 m s1) and frequent wind reversals promote small scale circulation and inertial waves. This breaks summer stratification and provides oxygen to the bottom waters in the zone located around the plume area (Estournel et al., 1997, 2001). Therefore in the Rhône coastal region, stratification occurs during summer warming, but it is counteracted by secondary windinduced circulation, which maintains high oxygen levels. 4.2. Nutrient and organic matter discharge As hypoxia is the result of the interplay between oxygen supply from surface water and atmosphere, and oxygen consumption from degrading organic matter, nutrient inputs which generate algal production and subsequent settling to the bottom waters are important forcing factors on the system. River estuaries and deltas are regions of very high productivity sustained to a great degree by nutrients of terrestrial origin. In this section, we examine nutrient discharge, and N:P and N:Si nutrient ratios (where available). We also examine the delivery of particulate and dissolved organic matter and their role in oxygen consumption. 4.2.1. Nutrient inputs and nutrient ratios of the river discharge In all four systems, the nutrient concentration in the river input is high during all seasons (Table 5). Indeed, DIN concentrations are around 100 mM on average for all systems, while DIP concentrations are much more variable. DIN and DIP input fluxes (Table 2) are related to water discharge and are maximal for the Mississippi and Changjiang and lower for the Pearl and Rhône Rivers. Riverine nutrient input fuels high primary production in the adjacent coastal zone. The nutrient load is generally associated with impacts in the estuary and surrounding waters as it is the total quantity of nutrients delivered, and its utilization by the ecosystem, which ultimately controls the total production of the delta and coastal system. Positive correlations exist between DIN load and primary productivity for the Mississippi (Lohrenz et al., this issue). Therefore, for determining the magnitude of potential hypoxia, the total flux of nutrients is a primary driver of the algal biomass formed and the potential oxygen consumption in bottom waters. However, differences in the timing of nutrient delivery, the nutrient concentrations, and nutrient ratios can significantly affect the amount and pattern of primary production. We therefore use nutrient concentrations and nutrient ratios to compare the formation of hypoxia in these four river-coastal systems with different discharge volumes. Data from a suite of studies assessing nutrient limitation of phytoplankton production (summarized in Rabalais et al., 2002) indicate that, in the case of the Mississippi, either N, P, or Si can limit phytoplankton growth, depending on the physical and biogeochemical conditions. In fact, N limitation appears most common during low flow periods and at higher salinities, particularly during late summer and autumn. Nitrogen is generally believed to be the main limiting nutrient, due to efficient recycling of P and loss of N through denitrification (Rabalais et al., 2002). During spring and early summer, P may play an important role in limiting primary production, especially in low and intermediate salinity regions of the plume. Evidence ARTICLE IN PRESS 1534 C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 from nutrient ratios and bioassays show that P limitation can occur during high flow and at intermediate salinities (Smith and Hitchcock, 1994; Lohrenz et al., 1997; Lohrenz et al., 1999; Sylvan et al., 2006). Models (Justic et al., 2002; Scavia et al., 2003; Turner et al., 2005) have utilized statistical relationships between hypoxia and riverine nutrient inputs to the shelf to predict or hindcast hypoxia. These models reinforce the view that nutrient stimulated production from the Mississippi and Atchafalaya Rivers drives the development and maintenance of coastal hypoxia. Si limitation is more variable and most pronounced in the spring (Dortch and Whitledge, 1992). Si limitation impacts diatoms (Nelson and Dortch, 1996; Lohrenz et al., 1999; Rabalais et al., 1999), which are an important fraction of the biomass of sinking particles (Redalje et al., 1994). Hence, Si dynamics are believed to be especially relevant for hypoxia formation (Turner et al., 1998; Dortch et al., 2001). In the Pearl River during the summer, nutrient loads are high due to inputs from the river (DIN 100 mM, DIP 1 mM, and DSi 100 mM) and rain (DIN 50 mM, DIP 1 mM, and DSi 50 mM) (Yin and Harrison, this issue; Yin et al., 2000, 2004b). The nutrient ratio of 100N:100Si:1P is about 7 times the Redfield ratio required for phytoplankton growth and hence P potentially limits biomass production in the summer (Yin et al., 2000, 2004b; Yin 2002, 2003). The Pearl is similar to the Mississippi since Si limitation may occur before the river discharge begins to increase in May and potential N limitation may occur in the winter dry season due to the monsoon-driven invasion of coastal water. This is also the case for the Rhône and Changjiang Rivers where the DIN:DIP ratio is also clearly higher than the utilization ratio (16:1). In contrast, the DIN:DSi ratio is close to the utilization ratio (1) which indicates that Si may not be limiting, except in the case of the Rhône River. However, these patterns, based on annually averaged concentrations, are only indicative of the potential limiting nutrient, as concentrations and phytoplankton species vary during the seasons and might provide different situations for different seasons. The pattern of nutrient limitation seems to be uncorrelated to the occurrence of hypoxia as Changjiang and Rhône (for example) are both strongly limited by P but only ECS close to the Changjiang undergoes summer hypoxia. Regeneration processes are crucial for transporting nutrients as part of the buoyant plume that forms from the discharging river water. In the case of the Mississippi, respiration accounts for 65% of the fate of the fixed carbon in the plume (Green et al., 2006) and recycling of plume nitrogen is a major pathway for nitrogen flow (Cotner and Gardner, 1993; Gardner et al., 1994). This nitrogen recycling and associated production of organic matter provides an important mechanism for transporting a portion of the river nitrogen load and resultant organic matter production to the shallow regions susceptible to hypoxia development. Because ratios of N, P, and Si have changed in most rivers during the past 50 years due to changes in land use, and dam building, the limiting nutrient has likely shifted also. For example, P limitation is likely more important now because of increased N input from the Mississippi River over the past 50 years (Turner and Rabalais, 1991). Nitrogen inputs have also increased in the Changjiang (Zhou and Shen, this issue) and other coastal areas of China (Harrison et al., 1990) over the last few decades. For the Rhône, nitrogen has increased during the seventies and stabilized since the early 1980s (Moutin et al., 1998). 4.2.2. Phytoplankton productivity, community structure, export and respiration As the river mixes with the coastal water, light conditions improve through dilution and sinking of large lithogenic particles and particulate organic material, and phytoplankton growth increases dramatically (Dagg and Breed, 2003). In the Mississippi, phytoplankton growth rates approach the theoretical maxima in the mid-salinity region, and can be as high as 3 d1 at summer temperatures of 30 1C (Fahnenstiel et al., 1995). In this region, primary production can reach 10 g C m2 d1 (Lohrenz et al., 1999) during early summer. Both grazing and dilution by physical mixing tend to reduce phytoplankton abundance, but the growth rates typical of mid-salinity regions are so high that phytoplankton biomass rapidly accumulates in spite of these loss terms (Lohrenz et al., 1999). These high stocks of phytoplankton are often visible in satellite images (Lohrenz et al., this issue). Large phytoplankton cells are subject to lower grazing mortality in the low- and mid-salinity regions because of the relatively slow numerical response by their major grazers, the copepods (Liu and Dagg, 2003). Consequently, large cells, especially diatoms, typically dominate the phytoplankton community in the mid-salinity region of the plume where sinking of organic matter is most intense (Bode and Dortch, 1996; Green et al., 2006). In the Pearl River estuary during the summer, large chainforming diatoms such as Skeletonema, Thalassiosira and Chaetoceros dominate and Chl a can range from 20 to 4100 mg m2 (Yin 2002, 2003) with the highest concentrations observed at the seaward edge of the plume. The Pearl River estuary is very productive with values ranging from 1 to 5 g C m2 d1 due to high surface temperatures of about 27 1C (Yin et al., 2000). The fate of this fixed carbon is not well understood in terms of how much sinks and how much is grazed by zooplankton. For the Rhône River, a contrasting situation is found. The primary production encountered in the transition zone between the near- and mid-fields is much lower (o1 g C m2 d1) than for the other three river systems, although the structure of the ecosystem is similar. Within the turbid plume where production is low, 50% of the chlorophyll a and 80% of the primary production is attributed to pico- and nanoplankton (Videau and Leveau, 1990; Pujo-pay et al., 2006). In the transition area between the plume and the marine system, microplankton represents 50% of the chlorophyll a and primary production, largely due to diatoms during spring. Primary production in the Changjiang-influenced coastal zone ranges from 1.5 to 4.5 g C m2 d1 (Chen et al., 2004) during summer. This high primary production is highly seasonal with values falling to 0.04 g C m2 d1 during winter (Chen et al., 2001). During summer, primary and new production is largely driven by diatoms in the coastal zone influenced by the river. In the case of the Changjiang, coastal upwelling plays an important role in supplying phosphorus-enriched shelf water to the surface waters during the summer (Chen et al., 2004). In the turbid area of the plume, flagellates may photosynthesize and accumulate due to their ability to swim upward during the day (Chen et al., 2003). The source of the organic load fueling hypoxia in the Changjiang coastal zone, whether it is from in situ production or organic matter advected from outside the plume, is currently under debate (Wei et al., 2007). Except in the case of the Rhône River, high primary production during spring and summer (1–10 g C m2 d1) is due to large fastgrowing diatoms, which can be exported through direct sinking at the end of the bloom, and contribute to large inputs of labile organic matter to bottom waters and sediments. Large phytoplankton cells can sink at rates of several meters per day, and aggregates of cells or mixtures of cells and detritus at rates of 10–100 m d1. At these rates, direct sinking of phytoplankton from the most productive layer of the plume, typically only 1–10 m thick, can easily provide a large enough input of organic matter to the sub-pycnocline layer that fuels hypoxia formation. Rapidly sinking fecal pellets provide an additional source of organic matter to the sub-pycnocline layer (Breed et al., 2004). ARTICLE IN PRESS C. Rabouille et al. / Continental Shelf Research 28 (2008) 1527–1537 If a significant fraction (50%) of the 5 g C m2 d1 reaches the sediment or bottom waters, this may cause large oxygen consumption in bottom waters. Up to 200 mmol m2 d1 of oxygen could be consumed, which may create hypoxia in days to weeks if the replenishment of oxygen through the pycnocline is decreased by stratification. As an example, vertical flux of organic carbon in various parts of the Mississippi River plume is as high as 1.80 g C m2 d1 during spring, but rates are lower during other seasons (0.29–0.95 g C m2 d1), and even lower away from the immediate plume (0.18–0.40 g C m2 d1) (Redalje et al., 1994). This vertical flux is equivalent to approximately 10–25% of phytoplankton production in mid-salinity regions of the plume (Breed et al., 2004). Amon and Benner (1998) calculated that bacterial oxygen consumption alone could reduce the oxygen concentration to hypoxic levels within 1–7 weeks during the summer. Chin-Leo and Benner (1992) calculated that 26–56 days of sub-pycnocline respiration (excluding benthic respiration) could lead to hypoxia. Large benthic oxygen demands ranging from 20 to 50 mmol O2 m2 d1 (Morse and Rowe, 1999) indicate that the sediment may constitute a large sink of oxygen. Dortch et al. (2004) suggested that bottom water oxygen depletion through both water and benthic respiration would take about 1 month in the summer. These different calculations indicate that organic matter mineralization into the sub-pycnocline layer is sufficient to consume oxygen and create hypoxia if oxygen is not replenished. 4.2.3. Doc and poc loading: what is their role in generating/ sustaining hypoxia? The contribution to hypoxia of organic matter directly discharged by rivers remains poorly quantified, but evidence from the Mississippi indicates it is small for this river-shelf system (Green et al., 2006). Most of the POC from the river is deposited close to the river mouth. Contrary to the paradigm of the terrigenous organic matter being largely refractory, this organic matter can be remineralized in the sediment giving rise to large oxygen demands (Morse and Rowe, 1999; Lansard et al., this issue). Sediment oxygen demand created by the direct deposition of organic matter can add to the oxygen demand generated by the settling of local primary production, reaching a threshold which might trigger hypoxia in bottom waters. Even less clear is the role of DOC in generating hypoxia. A fraction of the DOC from rivers is believed to be degradable, but largely degraded in estuaries (Raymond and Bauer, 2001) although Benner and Opsahl (2001) estimated that only 2–4% of Mississippi DOC is labile and would thus contribute to oxygen consumption when entrained in coastal bottom waters. Processes such as adsorption on particles (minerals or organic) in the water column can contribute to this transfer, but little is known about these processes near the river mouth. Cross-pycnocline exchanges will also promote the introduction of labile DOC in bottom waters together with oxygen, thereby reducing the net oxygenation of the waters. 1535 our comparison to properly evaluate this process. Physical constraints such as summer thermohaline stratification and long residence time are required for maintaining the isolation of bottom waters for hypoxia to occur. Broad intermediate-depth shelves (40–50 m) are also a precondition where tidal and wind mixing are damped and where intense pelagic–benthic coupling operating in the vertical transport of the algal biomass to depth. The Mississippi and Rhône Rivers and their shelves are at the two extremes of this classification: the Mississippi system has a long residence time, strong summer stratification, a broad intermediate-depth shelf and high primary production in its plume. This system currently displays the largest area of seasonal hypoxia among the four systems compared. Mediterranean waters close to the Rhône River have short residence time, summer stratification can be broken by wind reversals, primary production on the shelf is low and the shelf is deep. Therefore, it shows no evidence of hypoxia. The Changjiang and adjacent ECS are intermediate with a broad shelf, strong summer stratification and high primary production, but also high advection of water from the southern shelf, which makes summer hypoxia less persistent and less recurrent. The Pearl River estuary is shallow (o15 m) and wind and tidal mixing can reduce stratification. It has a short residence time and high flushing during the summer due to the high water discharge, and hence little hypoxia occurs in the lower estuary. The importance of the physical constraints on the occurrence of hypoxia points towards a potential risk of an increase in hypoxic area in a changing climate. Indeed, warmer summers and weaker winds, or changes in coastal water circulation, could lead to enhanced stratification or decreased open-water intrusion on the shelf. This could lead to an increase vulnerability to hypoxia in coastal areas, which are, at present, impacted by high nutrient discharge, but have sufficient summer mixing to prevent complete oxygen consumption. Acknowledgments We thank the organizing committee (our co-authors M. Dagg, M. Dai, and P. Harrison) of the symposium ‘‘Coastal Ecosystem Responses to Changing Nutrient Inputs from Large Temperate and Sub-tropical Rivers’’ held at Xiamen University (China) for inviting us to the meeting. C.R. acknowledges the funding by the ANRCHACCRA program (ANR-06 VULN-001-01) and the help of B. Bombled for figure design. M.H.D. acknowledges funding from NSF-China through Grant # 40576036. P.J.H. and K.Y. acknowledge funding from UGC (Project no. AoE/P-0404) and RGC (P-04-02) from the Hong Kong Government and NSFC 40676074 and 40490264. K. Yin and W.-J. Cai acknowledge the project supported by CAS/SAFEA International Partnership Program for Creative Research Teams. 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