YUAN Chengyi,WANG Yuheng,and WEI Hao,

1) College of Physical and Environmental Oceanography,Ocean University of China,Qingdao 266100,P.R.China

2) College of Marine Science and Engineering, Tianjin University of Science and Technology,Tianjin 300457,P.R.China

1 Introduction

In the central area of the Yellow Sea (YS),the phytoplankton bloom is a prominent event in spring (Fuet al.,2009; Zheng and Wei,2010).The quantities,ratios,and chemical compositions of nitrogen,phosphorus and silicon can strongly influence the composition,extent and duration of phytoplankton blooms,in addition to the hydrodynamical conditions,weather conditions and internal cycle of the ecosystem (Bodeet al.,2005; Carstensenet al.,2007; Fuet al.,2009; Nakayamaet al.,2010).Because nutrients provide the material base for algae growth,they support high primary production of algae during the bloom.As a limiting factor,nutrient depletion plays an important role in the termination of bloom as shown in observations and model simulations (Kudoet al.,2000;Tsunogai and Wantanabe,1983; Zou,2001).The budgets of nutrients vary in different stages of the annual life cycle of phytoplankton.The analysis of budgets enables the quantitative assessment of contributions from relevant sources of nutrients,depending on both the external inputs and internal cycles in the ecosystem.The relative importance of various processes in the supply of nutrients during bloom can thus be identified.

The YS is a shallow marginal sea located between the mainland China and the Korean Peninsula,where the nutrients of land sources can be transported by atmospheric deposition (Chunget al.,1998) and by river runoffs (Zhang and Liu,1994) from both the western and eastern sides.The YS is also a semi-enclosed sea that opens to the Bohai Sea (BS) and the East China Sea(ECS),thereby exchanges of nutrients are substantially affected by physical factors,most notably the northward Yellow Sea Warm Current (YSWC) in winter (Hsueh and Yuan,1997) and the Changjiang Diluted Water (CDW) in summer (Wanget al.,2003).In the meantime,mass transport across the thermocline by turbulent entrainment can not be ignored (Weiet al.,2002).The spatial and temporal variations of sources and hydrodynamic effects add to the complexity in the budgets study.

The biogeochemical/ecological modeling studies for different regions have either confirmed knowledge de-rived from field observations or gained new insight regarding the mechanisms of the ecosystem (Moll and Radach,2003; Patsch and Kuhn,2008; Hu and Li,2009;Kuhnet al.,2010).In addition,if coupled with a hydrodynamic component,the models can simulate the influence of physical factors more realistically.In the YS,simple box models for nitrogen,phosphorus and silicon have been developed based on Biogeochemical Modelling Guidelines of the Land–Ocean Interactions in the Coastal Zone (LOICZ) (Gordonet al.,1996; Liuet al.,2003).By considering the influence of hydrodynamic conditions on nutrients sources and internal recycling,one or three dimensional coupled models have been applied to simulate the spatial distributions and the annual cycles of some nutrient species (Azumayaet al.,2001;Zhanget al.,2002; Tianet al.,2003).

In this study,a modified lower trophic ecosystem model named North Pacific Ecosystem Model for Understanding Regional Oceanography (NEMURO,Kishiet al.,2007) is coupled with a widely-used three dimensional hydrodynamic model,namely the Princeton Ocean Model (POM,Blumberg and Mellor,1987).The coupled model is used to analyze the budgets of nutrients and the contributions of different sources of nutrients for maintaining the algae growth.The original NEMURO is modified by adding the cycle of phosphorus in view of the observations that P-limitation may take place in the southwestern part of the YS (Liuet al.,2003).The coupled model is used to study the relationship between the physical and biological/chemical processes and to study the dynamics of lower trophic levels as a way complementary to observations.

2 Model Set-Up

2.1 Model Description

The modified NEMURO is coupled with the three dimensional hydrodynamic model (POM) for for the study area of BS and YS as shown in Fig.1.The model has a horizontal resolution of 1/18? in longitude/latitude (Guoet al.,2006).After a spin-up of 9 years,the hydrodynamic module is nested to a larger outer model to provide climatological flow and temperature fields for the biological module.

The biological module consists of two types of phytoplankton,three types of nutrients and biogenic organic materials.The original NEMURO (Kishiet al.,2007) is modified by adding phosphate (PO43?),particulate organic phosphorus (POP),and dissolved organic phosphorus(DOP) to the original 11 state variables (Fig.2).River inputs and atmospheric deposition constitute additional sources of nutrients.River inputs include NO3?,NH4+,PO43?and SiO32?from the Changjiang (Yangtze) River,Minjiang River,Yellow River,Yalujiang River,Huaihe River,Han River and Qiantangjiang River.These rivers either flow into the YS directly,or significantly influence the budgets of nutrients in the computational domain.The atmospheric wet and dry depositions are also included into the inputs of the nutrients species discussed above.The transport of nutrients across the thermocline through turbulent entrainment is parameterized with seasonal entrainment velocities based on a mixing layer model (Weiet al.,2002).The bottom of upper layer during winter is set at a depth of 50 m.The exchanges of nutrients with the neighboring waters are represented by the advection fluxes.Light intensity in the water column is calculated from historical transparency data.The monthly transparency and river discharge are obtained from ‘Marine Atlas of Bohai Sea,Yellow Sea and East China Sea’ (Chen,1992),while monthly river inputs and seasonal atmospheric deposition of nutrients are taken from published data (Zhang and Liu,1994; Zhang,1996; Zhanget al.,1997; Chunget al.,1998; Wanget al.,2003; Liuet al.,2003; Wuet al.,2003; Limet al.,2007).

Fig.1 Domain of study model and topography.Line 1 links Chengshan Cape and Changsangot; Line 2 is located at 33.5?N; CC is a cross section for the calculation of nutrients fluxes,located between the northeastern bank of the Changjiang River and Cheju Island.The 70-m isobath represents the edge of the Yellow Sea Trough.

2.2 Model Parameters

The optimum light intensity for small phytoplankton(PS) and large phytoplankton (PL) are specified to be 1.98 W m?2s?2and 2.32 W m?2s?2,respectively,fully within the accepted ranges of 0.35–2.32 W m?2s?2(Parsonset al.,1984).The half saturation constants are set to 2.0 and 1.0 μmolN L?1for PL and PS of nitrate,and 0.3 and 0.1 μmolN L?1for PL and PS of ammonium,respectively; these values are within the range of 0.04–4.21 μmolN L?1for nitrate and close to the value of 1.30 μmolN L?1for ammonium observed in the eutrophic layer of the sub-arctic Pacific (Parsonset al.,1984).A half saturation constant of 2.0 μmolSi L?1is used for silicic acid.The half saturation constants of phosphate are 0.3 and 0.2 μmolP L?1for PL and PS,respectively.

The following decomposition rates are used: 0.01 d?1for the particle organic nitrogen (PON) to ammonium and dissolved organic nitrogen (DON); 0.02 d?1for DON to ammonium; 0.005 d?1for POP to phosphate and DOP;0.01 d?1for DOP to phosphate; and 0.01 d?1for Opal to silicate (Matsunaga,1981; Goodayet al.,1998).

The rates of mortality are set to 0.029 μmolN L?1d?1for large phytoplankton and 0.0585 μmolN L?1d?1for zooplankton and small phytoplankton,respectively.The other built-in parameters are the same as in the original model (Kishiet al.,2007).

Fig.2 Schematic view of the modified NEMURO model in lower trophic ecosystem.Boxes represent functional compartments,e.g.,small phytoplankton or nitrogen concentration.Arrows represent the fluxes of nitrogen (black),phosphorus (red) and silicon (blue) among state variables.River input,atmospheric deposition and exchange with the neighboring regions are shown as external sources of nutrients.

Fig.3 Monthly mean chlorophyll-a in the BS and the YS during an annual cycle.

3 Simulated Seasonal Cycles

3.1 Phytoplankton Biomass

Fig.3 shows the distribution of the monthly mean chlorophyll-aobtained from the model simulation.Relatively high concentration (>2 mg m?3) first appears in the central YS in the early March; peaks in April and lasting for more than five months.During March-July,highconcentration areas gradually extend to the entire southern YS; the concentration increases as the water becomes more stratified and decreases due to the consumption of nutrients.Starting from August,both the water temperature and the level of nutrients decrease; the concentration of chlorophyll-adecreases and it reaches the lowest value in winter.This annual cycle of chlorophyll-ain the YS can be divided into three phases,i.e.,spring bloom,post spring bloom and winter background periods,which will be discussed in details in Section 3.3.

The timing and spatial pattern of the formation and dispersion of high chlorophyll-aconcentration during March–May in the central YS,obtained from the model,are similar to those shown in the monthly sea surface chlorophyll-aderived from multi-year (1998–2009) observations by satellite remote sensing (Xuanet al.,2011).In general,the concentration of chlorophyll-ain the central YS reaches the highest value in spring,maintains a relative high level during summer,and then,decreases significantly in autumn and winter.The model-simulated seasonal variation is similar to the corresponding climatology of primary productivity shown in the Marine Atlas of Bohai Sea,Yellow Sea and East China Sea (Zhang,1991).

3.2 Nutrients

Figs.4–7 show the simulated seasonal variations of four types of nutrients.The concentrations of N,P and Si compounds are high in coastal areas of the YS,especially in the southwestern region.Such a general pattern is consistent within-situobservations (Liuet al.,2003; Wang,1991; Wanget al.,2003).The offshore region receives no direct river inputs and maintains relative higher primary production,thus leading to a lower nutrient level.During winter,the concentrations of phosphate and silicate in the southeastern region (especially near Cheju Island) are higher than those in the central YS because of the inputs from the ECS by the YSWC.The higher concentrations near the coast in the southern region are related to the influence of the CDW.

The highest concentrations of nutrients appear in February,which is considered as the final stage of the winter background period.After that,the water becomes more stable as the temperature increases,and the high levels of nutrients support the peaking of phytoplankton biomass during the spring bloom.During the post bloom period,the nutrients are gradually consumed by the growth of phytoplankton and they reach the nearly steady state in July.Most of nutrients have been converted into the standing crops of phytoplankton and zooplankton.After September,because the stratification becomes weaker as the wind mixing gets stronger,thus,enabling significant transport of nutrients across the thermocline,the vertical transport is combined with horizontal imports from the ECS,leading to gradual increase in the levels of nutrients during the winter background period.

Fig.4 Monthly mean nitrate in the BS and the YS during an annual cycle.

In the central YS,the model produces similar spatial and temporal variations of the concentrations of nutrients as compared within-situobservations (Wanget al.,2003).For phosphate,the concentration is in the range of 0.3–0.5 μmol L?1in January,gradually decreases to lower than 0.3 μmol L?1in May and lower than 0.1 μmol L?1in August,and then increases to the range of 0.1–0.3 μmol L?1in November.These ranges favorably agree with thein-situobservations.For silicate,the concentration is the lowest in August and the highest in January in the central YS.For nitrate and ammonium,the seasonal variations of their concentrations from the present model are also consistent with the observations and the results of other model simulations (Zhao and Guo,2010).

Fig.5 Same as Fig.4,except for ammonium.

Fig.6 Same as Fig.4,except for phosphate.

Fig.7 Same as Fig.4,except for silicate.

3.3 Chlorophyll-a and Nutrients in the Central YS

The sub-region of the central YS is enveloped by the 50 m isobath,Lines 1 and 2 shown in Fig.1.The modeling reaches a stable state after a spin-up of 9 years.Fig.8 shows the annual cycles of chlorophyll-aand nutrients in the central YS obtained by the model.

The annual cycle can be divided into different phases.Different definitions of phytoplankton bloom have been used in previous studies.Siegelet al.(2002) and Henson and Thomas (2007) defined the initiation of the bloom as the observed chlorophyll-arises to 5% above the annual median value and remains elevated for at least three days.As the simulated variation in the central YS is quite smooth (Fig.8),we simply define the initiation of the bloom as the chlorophyll-arises to 5% above the annual median value.The starting of the winter background period is defined as the chlorophyll-adrops to 5% below the annual median value.

According to the definitions above,the modeling results suggest that the spring bloom period begins in the mid-March and ends in the early July,lasting less than 4 months; the post spring bloom period begins in the early July and ends in the early September,lasting 2 months;the winter background period begins in the September and ends in the March of the next year,lasting more than 6 months.

Fig.8 Annual cycles of (a) chlorophyll-a,(b) nitrate and ammonium,(c) phosphate and (d) silicate in the central YS.

In the central YS,during the winter background period,because both temperature and light intensity are not favorable to phytoplankton growth,there is little consumption of nutrients.Meanwhile,external inputs caused by advection and vertical mixing are relatively high,thus the concentrations of all the nutrients species reach the highest point during this period.During the spring bloom period,because of the increasing temperature and the light intensity together with the huge amount of nutrient supply,occurs the highest phytoplankton growth.After going through the highest consumptions by photosynthesis of phytoplankton during bloom,the concentrations of nitrate,phosphorus and silicate drop to their minimum values at the beginning of the post spring bloom period.

4 The Budgets of Nutrients in the Central YS

4.1 Budgets of Different Stages During the Seasonal Cycle

The budgets of nutrients in the central YS are estimated through analyzing the modeling results,which are summarized in Figs.9–12.The contribution factors include atmospheric deposition,transport across thermocline,exchange with neighboring waters,and biological and chemical processes.The budgets are analyzed for each nutrient species,and for the winter background,spring bloom and post spring bloom periods,respectively.Overall,the largest sources of nutrients are the release from respiration; and the largest sinks come from the photo-synthesis of phytoplankton.The two fluxes are largely canceled out each other and their difference is regarded as the net consumption by phytoplankton in Figs.9–12.

Fig.9 Budgets of nitrate in the central YS for three periods coincided with the seasonal cycle of chlorophyll-a.WBP,SBP and PSBP denote the winter background,spring bloom and post spring bloom periods,respectively.The percentages stand for the contributions of various processes.The concentrations and fluxes of nutrients are in units of μmol L?1 and 109 mol year?1,respectively.Positive and negative numbers of fluxes denote sources and sinks,respectively.

Fig.10 Same as Fig.9,except for ammonium.

Fig.11 Same as Fig.9,except for phosphate.

Fig.12 Same as Fig.9,except for silicate.

During the winter background period,for nitrate,the exchange with neighboring waters provides 97% of the total source; and the transport across the thermocline contributes to 85% of the total sink.The exchange with neighboring waters also makes significant contributions to the total sources of ammonium and phosphate (37%and 50%,respectively).But for silicate,the primary source (60% of the total) comes from the transport from layers deeper than 50 m.Contribution from the exchange with the neighboring waters is less important because the concentration of silicate is relatively low in the YSWC.

During the spring bloom period,the exchange with neighboring waters provides the primary sources for nitrate,ammonium,phosphate and silicate,amounting to 93%,34%,54% and 65% of the totals,respectively.Transport across the thermocline makes significant contribution to the sources of phosphate and silicate,amounting to 33% and 24% of the totals,respectively.

During the post spring bloom period,the relative importance of the processes differs for various nutrient species.Similar to the other two periods,the exchange with neighboring waters is the primary source for nitrate.For ammonium,the atmospheric deposition,excretion and decomposition make similar contributions to the sources.For phosphate and silicate,the primary sources are the transport across the thermocline,amounting to 62% and 68% of the totals,respectively.In general,the net consumption by phytoplankton makes the primary contribution to the sink of nutrients.

4.2 Contribution of External Processes

Averaged annually,the external processes contribute 3.8×1011,1.9×1010and 9.6×1010mol,i.e.,more than 90%,to the total sources of nitrate,phosphate and silicate,respectively.For ammonium,the external processes provide 1.6×1010mol,i.e.,42%,to the total source,similar to the contribution from the internal processes.

Atmospheric deposition makes significant contribution to the entire region,especially in the central YS that is away from direct influence of rivers (Zhang and Liu,1994; Chunget al.,1998; Liuet al.,2003).Averaged annually,atmospheric deposition is of similar importance as the exchange with neighboring waters to ammonium.For silicate,the contributions from atmospheric deposition,exchange with neighboring waters and supplement across the thermocline are of similar importance during the post spring bloom period.For all the other situations,the contributions from atmospheric deposition are one or two orders of magnitude smaller as compared with those from the exchange with neighboring waters or transport across the thermocline (Figs.9–12).

Horizontal advection and exchange lead to the smoothness in the spatial distributions of nutrients,and influence the annual cycles and the horizontal patterns of nutrients(Moll and Radach,2003; Weiet al.,2004).River input has direct influence in the estuarine area,and can be transported to the central YS by advection (Zhang and Liu,1994).For nitrate,import from neighboring waters is one or two orders larger than atmospheric deposition if considering the magnitude and its transport across the thermocline,especially during the winter background period,suggesting the significant role played by the YSWC.For other nutrient species,the horizontal exchange is comparable to other external processes (Figs.10– 12).

For phosphate and silicate,the transports across the thermocline provide 8.0×109and 5.5×1010mol over the entire year,playing the primary (Fig.11) or secondary(Fig.12) roles in their replenishment,respectively.The inputs by transporting from the layer deeper than 50 m reach the maximum magnitudes during the winter background period,corresponding to the largest entrainment velocity and the relatively large difference in the concentration between the upper and lower layers (Weiet al.,2002).

4.3 Contribution of Internal Processes

Respiration and photosynthesis of phytoplankton provide the largest source and sink among the internal processes (Wanget al.,2002).Their differences,regarded as the net consumptions by phytoplankton,are the primary sink in most situations except for nitrate during the winter background period.Averaged annually,the net consumptions by phytoplankton are 3.2×109,4.1×1010,1.5×109and 1.9×1010for nitrate,ammonium,phosphate and silicate,respectively.During the spring bloom period,in particular,the net consumptions by phytoplankton contribute to more than 93% of the total sinks for all the species of nutrients.

For ammonium,internal processes including decomposition and excretion provide 2.2×1010mol over the entire year,accounting for 58% of the total sources.For all the periods,internal processes contribute to more than 50%of the ammonium replenishment.As a transformation process of nitrogen,the nitrification of ammonium accounts for 24% of the total sink during the winter background period,hence it is non-negligible.

4.4 Nutrients’ Ratios

The algal N/P ratios of nutrient saturation vary between 8 and 27 with an average 16 for marine species (Sakshaug and Olsen,1986).Deviations from these typical values indicate whether the nutrient becomes the limiting factor in the algae growth.The average N/P ratio in the southern YS is up to 51.8,indicating the possible P limitation in this region.The average N/P ratio in the central YS is around 29.0,closer to the typical values for phytoplankton composition.

The f-ratio is a proxy ratio between the new production and total production (Eppley and Peterson,1979).The average f-ratios in the southern and central YS are 0.6 and 0.3,respectively.This suggests that more primary production is fuelled by nitrate (referred to as the new production) in the southern YS,due to the direct or indirect influence of river inputs.

5 Exchange with the ECS Through Section CC

The YS and ECS are separated by the section CC linking the northeastern bank of the Changjiang River and Cheju Island (Fig.1).The fluxes of nutrients across this section quantify the contribution of sea water circulation and river inputs for the nutrients in the YS.The section CC can be further divided into western and eastern parts by the isobath of 50 m that represents the boundary of the CDW extension and the YSWC.

Averaged annually,the inputs of nutrients across the section CC could reach up to 2.0×1011,1.0×1011,8.7×109and 5.2×1010mol for nitrate,ammonium,phosphate and silicate,respectively.During different periods of the annual cycle,the inputs of nutrients across the western and the eastern parts of section CC are generally positive,i.e.,acting as sources of nutrients for the central YS (Table 1).Exceptions,i.e.,nutrients exporting from the YS to the ECS,are nitrates during the post bloom period across the eastern section and ammonium during the winter background period across the western section.Averaged annually,more nitrates are imported to the YS across the western than across the eastern section.

According to the modeling results,during spring and summer,high N/P ratios (>30) are found in the Changjiang estuary and its adjacent areas,including the southern and southwestern parts of the YS,inshore area of the ECS,and the area to the east of the Changjiang estuary.These characteristics are consistent with field observations(Wanget al.,2003).From Table 1,the N/P ratios of the transported water across the western section could reach up to 39 and 70 during the bloom and the post bloom periods,respectively.These high ratios indicate the influence of terrestrial runoff,especially the Changjiang River runoff.During the spring bloom period,the fluxes of all the nutrients across the western section are larger than those across the eastern section.This also indicates the influence from the CDW.During winter with northerly winds,the CDW hardly flows across the western part of section CC,thus,the N/P ratio turns to be relatively small(around 31) during the background period.

The N/P ratios in the water flowing across the eastern section are 6 and 2 for the background and the bloom periods,respectively.These ratios are much smaller than the corresponding values across the western section.During winter,the fluxes across the eastern section represent the ECS offshore water that is imported to the YS by the YSWC.During the winter background period,the inputs by the YSWC are estimated to be 4.6×1010,2.3×1010,2.0×109and 1.2×1010mol for nitrate,ammonium,phosphate and silicate,respectively.

Table 1 Fluxes of nutrients of the entire section CC,the western portion and the eastern portion of section CC (unit: 109 mol year?1) for the periods WBP,SBP and PSBP

6 Conclusions

Besides considering the river inputs and atmospheric depositions,the original NEMURO model has been modified by including the phosphorus cycle and coupling with a hydrodynamic model for its application in the YS.In general,the simulated horizontal distributions,and annual cycles of chlorophyll-aand the nutrients well agree with observations.

The analyses of budgets reveal that the relative importance of different processes varies for specific nutrients species during different periods of the annual life cycle of phytoplankton.During the winter background period,the inputs by exchanging with neighboring waters are the primary sources for nitrate,ammonium and phosphate;but the primary source of silicate is from the layer deeper than 50 m,contributing to 60% of the total input.During the spring bloom period,the exchange with neighboring waters makes the most significant contribution for all the nutrients,and the transport across the thermocline makes significant contributions for phosphate and silicate.During the post spring bloom period,the relative importance of different processes varies for specific nutrients.The exchange with neighboring waters plays the most important role in the replenishment of nitrate.Atmospheric deposition,excretion of phytoplankton and decomposition make similar contributions to ammonium.For phosphate and silicate,the input by transport across the thermocline contributes 62% and 68% to the total sources,respectively.

The annually averaged N/P ratio over the whole southern YS is 51.8,indicating the potential P limitation in this region.The average N/P ratio in the central YS is 29.0,closer to the typical values of phytoplankton composition.Generally,the fluxes across section CC in Fig.1 provide important sources of nutrients in the YS,suggesting the importance of the water exchange with the ECS,which is influenced by the large scale sea water circulation.During the bloom and the post bloom periods,the N/P ratios in the transported water across the western part of section CC are affected by the CDW with high N/P ratios.During the winter background and the bloom periods,the N/P ratios are much lower for sea water across the eastern section,indicating the influence of the YSWC.

The present study focuses on climatological seasonal cycles.The inter-annual variations of hydrodynamic conditions,nutrients and related external processes will be the subjects of our upcoming study.

Acknowledgements

This study was funded in part by the Chinese Ministry of Science and Technology under Contract Nos.2006CB 400602 and 2011CB403606 and in part by the key program from the National Natural Science Foundation of China under Contract No.40830854.We would like to express our thanks to Dr.Guo Xinyu from Ehime University for providing the relevant results of POM model and to express our gratitude to Dr.Zhao Liang from Ocean University of China for helpful guidance; we also appreciate the insightful comments from the reviewers who provided very helpful idea for improving the manuscript.

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