L
Journal of Experimental Marine Biology and Ecology 249 (2000) 111–121
www.elsevier.nl / locate / jembe
Experimental examination of the effects of atmospheric wet
deposition on primary production in the Yellow Sea
a ,* a a,b
L. Zou , H.T. Chen , J. Zhang
a
College of Chemistry and Chemical Engineering, Ocean University of Qingdao, 5[Yushan Road,
Qingdao, 266003, P.R. China
b
State Key Laboratory of Estuarine and Coastal Dynamics, East China Normal University, 3663[Zhongshan North Road, Shanghai, 200062, P.R. China
Received 11 February 1999; received in revised form 29 February 2000; accepted 2 March 2000
Abstract
The effects of atmospheric wet deposition on primary production in the coastal Yellow Sea were examined by in situ incubation experiments in August, 1997. Phytoplankton species flourished in response to nutrient additions and chlorophyll-a (Chl-a) increased significantly when rainwater was added. Concentration of Chl-a increased 2.6 times with the addition of 10% (v / v) rainwater. In a coastal eutrophic region like Jiaozhou Bay, the impact of atmospheric wet deposition is negligible. However, the N / P ratio ranged from 22:1 to 80:1, indicating P limitation of photosynthesis in the Yellow Sea. During field observations, high N and low P rainwater was observed to be transported into the oligotrophic central Yellow Sea. Ammonium was used by phytoplankton in preference to nitrate, and Fe stimulated nutrient uptake by phytoplankton. Rainwater increased the Chl-a growth more than a single nutrient owing to the abundance of both plant and trace nutrients in the rainwater. A negative exponent relationship may exist between the impact of rainwater and total nutrient quality of the water in influencing phytoplankton growth.
2000 Elsevier Science B.V. All rights reserved.
Keywords: Rainwater; Chlorophyll a; Photosynthesis; Jiaozhou Bay; Yellow Sea
1. Introduction
The atmosphere is an important route for the transportation of nutrients into the marine environment, especially in those short of riverine, upwelling and oligotrophic regions (Menzel and Spaeth, 1962; Paerl, 1985, 1993; Duce, 1986; Loye-Pilot et al.,
*Corresponding author. Tel.:186-532-203-2005; fax:186-532-296-3005.
E-mail address: [email protected] (L. Zou)
1990). Studies in N-limited estuarine, coastal and oceanic waters show that the marine primary production is stimulated by N compounds of wet and dry forms from atmospheric discharge (Thayer, 1974; Pael et al., 1990, 1999; Willey and Cahoon, 1991; Willey and Paerl, 1993; Paerl and Fogel, 1994; Peierls and Paerl, 1997). Moreover, rainfall produces a greater stimulation than either ammonium or nitrate when the amount of N is considered (Pael et al., 1990; Paerl and Fogel, 1994). This may due to the other elements in rainwater, which include P, Si, Al and Fe (Martin et al., 1989; Duce and Tindale, 1991; Duce et al., 1991). Since Fe is a component of the enzymes responsible for nitrate reduction to ammonium and N2 fixation (Stewart, 1974), the cooperation between Fe and N in enhancing marine primary production has been affirmed (Harrison et al., 1987; Martin et al., 1991; Ditullio et al., 1993; Pael et al., 1999).
The Yellow Sea is located in the northwestern Pacific Ocean, and has an oligotrophic character, which is somewhat similar to the central Pacific Ocean. Since input from rivers and upwellings are small, atmospheric deposition plays an important role for nutrients. Previous studies indicate that 65% dissolved inorganic nitrogen (DIN) and 70% dissolved inorganic phosphorus (DIP) can be delivered to the surface of the Yellow Sea via the atmosphere (Zhang and Liu, 1994). Rain-stimulated primary production is considered as a category of ‘new production’ due to the nutrient input to the system by atmospheric deposition. It is estimated that nitrate in precipitation contributes about 4.3–9.2% of the nitrate requirement for the annual new production in the Yellow Sea. Three times higher production would be expected if dry nitrate deposition, and wet and dry ammonium deposition are included (Chung et al., 1998).
On an average, episodic deposition of nutrient elements accounts for only a small fraction of the concentration in seawater. However, individual rain events are directly deposited on the sea surface and result in temporal eutrophication of surface waters. In this manner, chlorophyll a (Chl-a) and phytoplankton biomass in the surface water may be greatly increased over short periods (Owens et al., 1992; Mallin et al., 1993; Pearl, 1995), which may result in deleterious blooms (Zhang, 1994; Paerl, 1997).
Very limited data are available in the literature on the relative production between phytoplankton and atmospheric deposition. However, in this study we provide data from in situ observations on the effects of wet deposition on phytoplankton growth in the Yellow Sea during the summer, when stratification is dominant in the water column.
2. Materials and methods
2.1. Rainwater sampling
Fig. 1. Location of sample stations.
rainwater was determined by traditional colorimetric methods for seawater samples (Parsons et al., 1987).
2.2. In situ incubation experiment
Sample location sites are shown in Fig. 1. Sub-surface water samples were collected with a 5-l plastic sampler at A, C and D, and passed through a 180-mm mesh to remove large particles, and then transferred into 0.50-l incubation bottles. Triplicate samples were prepared for each nutrient / rain incubation group.
2.3. Incubation with rainwater
A 50-ml volume of rainwater was added to 450 ml of sub-surface water. Then the bottles were floated on the sea surface. The effect of salinity change was examined by incubation using 50 ml DDW and 450 ml seawater. The incubation experiment was carried out for 24 h.
2.4. Nutrients effects
Table 1
Methods of chemical analysis for nutrient species, including precision and detection limits (mM)
Species Methods Detection Precision
limits (%)
Nitrate Cd–Cu reduction 0.05 1.2
Nitrite Azo dye complex 0.02 0.5
Ammonium Indophenol blue complex 0.15 3.7
Orthophosphate Phosphomolybdate complex 0.03 0.6
Silicate Silicomolybdic complex 0.05 0.5
were prepared in the laboratory and stored at 48C. The unchelated FeCl solution was3 freshly mixed with Milli-Q water in situ prior to experimentation. All containers and tubing for storing and dispensing were made of polyethylene or natural rubber, soaked with 20% HCl for 24 h, washed by distilled water and then Milli-Q water. The following incubations were carried out for 24 h in the same manner as in the rain experiment.
In all experiments, control samples were prepared. After incubation, samples were filtered immediately through 0.45-mm pore-size filters and frozen until analysis. 2.5. Nutrient analysis
All experimental containers (e.g. incubation bottles) were rinsed in 10% HCl for 24 h and then rinsed thoroughly with DDW before use. Nitrate, nitrite, ammonium, orthophosphate and dissolved silicate were analyzed by classic colorimetric methods (Parsons et al., 1987). Detection and precision of the analyses are shown in Table 1.
2.6. Chlorophyll a analysis
Samples for Chl-a were filtered using Whatman GF / F filters. Particles on the filter were extracted with 90% acetone at 48C in the dark for 24 h. Chl-a concentrations were determined by a fluorometric method (Parsons et al., 1987).
3. Results
3.1. Nutrients
Concentrations of DIN (nitrate1nitrite1ammonium), DIP (orthophosphate) and DISi (silicate) in situ water samples and rainwater are shown in Table 2.
Station A is located within the Jiaozhou Bay, while station C and D are further offshore in the Yellow Sea. The results of the nutrient analyses show that the DIN concentrations ranged from 3.75 to 8.15 mM at these three stations. At station A, DIN was double the concentration compared with stations C and D, and DIN of station D was 30% higher than C. The DIP concentrations decreased from 0.36mM at station A to 0.06
Table2
Dissolved inorganic N:P and Si concentrations at three stations and for rainwater samples
Station A C D Rainwater
DIN (mM) 8.15 3.75 4.83 11.65
DIP (mM) 0.36 0.21 0.06 0.14
DISi (mM) 8.92 15.60 4.51 0.50
N:P:Si 22:1:25 18:1:74 80:1:75 83:1:3.5
over three times higher than that of station D, and the DISi at station A has a concentration almost double that of station D (8.92 mM compared to 4.51mM).
Compared with the nutrients in the seawater, the DIN concentration in the rainwater of 11.65 mM was much higher than the seawater samples. The DIP concentration in rainwater was lower than the samples from station A and C, but higher than that from station D. DISi in rainwater was 0.50mM, i.e., about 10% of that of the seawater from station D.
3.2. Chlorophyll a
The Chl-a concentrations are presented in Fig. 2. Concentrations of Chl-a in surface 23
water at stations A, C and D decreased from 2.68 to 0.08 mg m . The concentrations of Chl-a in nutrient and rainwater incubations at these three stations were compared to the batch control. At station A, Chl-a concentration for rainwater incubation was similar to
23
that of the control of 3.60 mg m . Chl-a concentrations under rainwater-amended conditions at station C and D were higher than those for the controls, especially at station D, where the Chl-a concentration was almost twice as high as the batch control. Changes in Chl-a concentration due to addition of nutrients (CN, changes due to nutrients) and rainwater (CR, changes due to rainwater) were estimated by the following equations and the results are shown in Table 3
CN5[(Chl-a)N2(Chl-a) )] / dose of nutrientC (1)
CR5[(Chl-a)R2(Chl-a) ] / rainwater doseC (2)
where (Chl-a) , (Chl-a) , and (Chl-a)N R C represent Chl-a concentration of incubations in nutrient, rainwater and control, respectively.
It is evident from Table 3 that the significant Chl-a increase in response to nutrient 23 additions takes place in the case of phosphate, ranging from 0.025 to 0.050 mg m , indicating P limitation for phytoplankton growth. With respect to DIN, Chl-a ranges
23 1 2
from 0.016 to 0.061 mg m for NH , while the incubation range for NO4 3 is from 23
0.006 to 0.029 mg m (Table 3). The phosphate limitation relative to nitrogen for Chl-a 32
is probably due to the low concentration of PO4 and the elevated N / P ratio (80:1) in this region. The effect of DISi on Chl-a was not as significant as that of the other plant
23
nutrients at these stations with 0.003 mg m . The influence of Fe was significant at 23
23
Fig. 2. Chl-a concentrations (mg m ) of start, control, nutrients and rainwater incubations in situ. Start, group at beginning of incubation; control group;1rain, group incubated under rainwater;1NO , group incubated3
under nitrate;1NH , group incubated under ammonium;4 1P, group incubated under phosphate;1Si, group incubated under silicate; Fe, group incubated under Fe(III).
Table 3
23 23 23 21
Chl-a concentration of start and control (mg m ), CN (mg m permM of nutrient) and CR (mg m l of rainwater)
1
Station Start Control NO3 NH4 P Si Fe Rainwater
A 2.68 3.60 0.014 0.016 0.050 20.003 20.82 21.20
C 0.17 0.72 0.029 0.061 0.045 0.005 0.040 3.80
D 0.08 0.10 0.006 0.018 0.025 0.006 0.025 3.80
Fig. 3. Relationship between EV and TQ. 23 21
CR was observed at station A, that is, 21.20 mg m l ; while significant but positive 23 21
CRs occurred at stations C and D, i.e., 3.80 mg m l .
Results of the effects of light on Chl-a concentrations are shown in Fig. 3. Concentrations of Chl-a were reduced when light radiation decreased.
4. Discussion
It has been reported that photosynthesis was phosphorus-limited in coastal waters of China (Zhang, 1988; Zhang, 1994), whereas nitrogen limitation probably takes place in Europe and in North American coastal waters (McCarthy et al., 1977; Willey and Cahoon, 1991; Mallin et al., 1993; Zhang, 1994). Our studies indicate that phyto-plankton is most likely P limited in the coastal Yellow Sea, which appears to be a result
32
of both low absolute PO4 concentration and a high N / P ratio (about 80:1). Wet deposition carries both phosphate and other limiting elements (e.g. Fe) to the Yellow Sea. Given that the N / P ratio in rainwater is 83 / 1, addition of rain to the surface seawater will further increase the N / P ratio.
The incubation with phosphorus shows that concentrations of Chl-a at station A, C, and D were increased to various degrees. The P limitation situation is alleviated followed by a phytoplankton biomass increase when P was added. Ammonium appears to be the more important limited nutrient compared to nitrate, and Chl-a in ammonium incubations were twice as high as that in nitrate incubations. The experimental data in this study are in agreement with previous studies that ammonium is preferred by phytoplankton over nitrate (Kanda et al., 1990).
solution in our incubation in situ led to a large increase in Chl-a concentration, which indicated again the special effect of Fe on the uptake of phytoplankton.
Chl-a concentrations in rainwater groups were 6.2% lower than that for the control in station A. This is most likely due to DIP dilution by the rainwater in the incubation water sample (0.30mM), although the DIN concentration was increased in the rainwater incubation experiment. Moreover, the N / P ratio in the rainwater was about 83 / 1, which is much larger than the 22 / 1 at station A. In contrast, DIP concentration at station C, diluted by rainwater, appeared positive. Chl-a concentration with rainwater incubation
23
was 0.19 mg m higher than the batch control. What could be the reason? First, the change of DIP concentration was only 0.01 mM (from 0.21 to 0.20 mM), which was quite limited compared to the absolute concentration of the batch control. Second, DIN concentrations were significantly increased from 3.75 to 4.54 mM by rainwater, so that phytoplankton species of station C may have a different composition and respond differently to nutrient level changes. At station D, both DIN and DIP significantly increased from rainwater, which increased the DIN concentration by 15% and the DIP concentration by 17%. Such a change in nutrient levels resulted in an increase of Chl-a twice as high as the batch control.
The experimental data show that phytoplankton growth (e.g. Chl-a) can be stimulated by single nutrient additions to various extents. Supposing that only nitrate, nitrite, phosphate and silicate are considered, then the effect of rainwater in changing the Chl-a concentration introduced by rainwater can be estimated by
2 1
where (Chl-a)NO3 represents the Chl-a change stimulated by 1 mM of nitrate; and
2 2
similarly for (Chl-a)NH4, (Chl-a) , and (Chl-a) . [NO ]P Si 3 rain represents NO3 con-1
centration in rainwater; similarly for [NH ]4 rain, [P]rain, and [Si]rain. (Chl-a)NO3?
2
[NO ]3 rain represents the change in Chl-a concentration affected by nitrate in rainwater and similarly for (Chl-a)NH4?[NH ]4 rain, (Chl-a)P?[P]rain and (Chl-a)Si?[Si]rain.
23 21 Compared with the effect of natural rainwater incubation (2.13 mg Chl-a m l ), the estimated changes of Chl-a affected by supposed rainwater is only one sixth of that from natural rainwater. It can be concluded that trace elements and organic materials in rainwater, which are under estimated in this study, could stimulate phytoplankton growth.
Furthermore, compare the effect of rainwater (EV, experimental value) and quality of surface water (TQ, total quality) shown in Fig. 3, and suppose that
EV5[(Chl-a)R 2(Chl-a) ] /(Chl-a)C S (4)
TQ5DIN?DIP?(Chl-a)S (5)
control and at the start. We concluded that there is a negative relationship between EV and TQ, which means that under the same rainwater environment, the lower nutrient condition station (station D), has a greater increase in Chl-a; while at the higher nutrient condition station (station A), there is less change in Chl-a compared to the control. Moreover, EV and TQ have a somewhat negative exponent relationship.
Solar radiation is an important factor for primary production (Nielsen et al., 1979; Ning et al., 1991). From the data in this experiment, it may be seen that the Chl-a concentrations appear to decrease with the lowering of the radiation. This can be brought into a broad concept that an increase in suspended matter concentration would dramatically reduce photosynthesis, as shown in Fig. 4. A non-linear relationship between radiation and Chl-a concentration has been identified. Chl-a concentrations
23
decreased from 1.00 to 0.73 mg m with a reduction in light intensity of 100 to 80%. When light intensity was reduced to 0% (i.e. black bottle incubation), Chl-a con-centrations were reduced to 42%.
The Yellow Sea receives a significant amount of nutrients via atmospheric deposition. Atmospheric wet deposition may represent 65 and 70% of total input for DIN and DIP nutrients, respectively (Zhang, 1994; Zhang and Liu, 1994). Nutrient-enriched rains could dramatically enhance marine bioproduction (McCarthy et al., 1977; Zhang, 1994). The production enhanced by rainwater is ‘new production’, which is especially important for oligotrophic waters, such as the central Yellow Sea.
Rainfall data are available from local authorities. Annual rainfall in the east coastal Yellow Sea averages 600–700 mm, of which 60–80% takes place in the summer season when the water column is stratified with DIN and DIP concentrations of 55.5 and 1.90
mM in rain (Zhang, 1994). This suggests that approximately 505 mg N and 2.8 mg P are put into the upper layer per square meter. Based on the Redfield ratio C:N:P5106:16:1,
22
a value of 115 mg C m of carbon fixation (new production) would be expected annually from the input of nutrients by rain.
5. Conclusion
The results of this study indicate that atmospheric wet deposition has an important effect on the phytoplankton growth in the Yellow Sea, and individual rain events may significantly stimulate photosynthesis. The nutrient input by rain temporally changes the absolute P concentration and N / P ratio in the surface layer of the coastal ocean. Under certain conditions (e.g. radiation and temperature), episodic rain events may lead to a flourish of phytoplankton in the Yellow Sea.
Acknowledgements
We gratefully acknowledge the financial support from the National Natural Science Foundation of China for grant funds Nos. 49576297, 49736190 and 49525809. We thank Professor William F. Grant, McGill University, Montreal, for linguistic improvements. Thanks was also given to Dr. Kan Zeng, Ocean University of Qingdao, for image edition. And the anonymous reviewers are acknowledged for the helpful comments and improvement of the original manuscript. [RW]
References
Behrenfeld, M.J., Bale, A.J., Kolber, Z.S., Aiken, J., Falkowski, P.G., 1996. Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383, 508–511.
Chen, C. et al., 1997. Effect of Fe(II) to the growth and ability of assimilating on nitrogen of Bacillariophyta (In Chinese). Acta Oceanol. Sin. 19 (3), 50–56.
Chung, C.S., Hong, G.H., Kim, S.H., Lim, J.H., Park, J.K., Yang, D.B., 1998. Shore based observation on wet deposition of inorganic nutrients in the Korean Yellow Sea coast. The Yellow Sea 4, 30–39.
Ditullio, G.R., Hutchins, D.A., Bruland, K.W., 1993. Interaction of iron and major nutrients controls phytoplankton growth and species composition in the tropical North Pacific Ocean. Limnol. Oceanogr. 38, 495–508.
Duce, R.A., 1986. The impact of atmospheric nitrogen, phosphorus and iron species on marine biological productivity. In: Menard, P. (Ed.), The Role of Air–Sea Exchange in Geochemical Cycling, D. Reidel, Berlin, pp. 497–529.
Duce, R.A., Tindale, N.W., 1991. Atmospheric transport of iron and its deposition in the ocean. Limnol. Oceanogr. 36, 1715–1726.
Duce, R.A., Liss, P.S., Merril, J.T., Atlas, E.L., Buat-Menard, P., Hicks, B.B., Miller, J.M., Prospero, J.M., Arimoto, R., Church, T.M., Ellis, W., Galloway, J.N., Hansen, L., Jickells, T.D., Knapp, A.H., Reinhardt, K.H., Schneider, B., Soudine, A., Tokos, J.J., Tsunogai, S., Wollast, R., Zhou, M., 1991. The atmospheric input of trace species to the world ocean. Global Biogeochem. Cycl. 5, 193–259.
Harrison, W.G., Platt, T., Lewis, M.R., 1987. F-ratio and its relationship to ambient nitrate concentration in coastal waters. J. Plankton Res. 9, 235–245.
Kanda, J., Ziemann, D.A., Conquest, L.D., Bienfang, P.K., 1990. Nitrate and ammonium uptake by phytoplankton populations during the spring bloom in Auke Bay, Alaska. Estuarine, Coastal Shelf Sci. 30, 509–524.
Liu, R., 1992. Ecology and Living Resources of Jiaozhou Bay, Science Publishing House, Beijing, (In Chinese).
Mallin, M.A., Paerl, H.W., Rudek, J., Bates, P.W., 1993. Regulation of estuarine primary production by watershed rainfall and river flow. Mar. Ecol. Prog. Ser. 93, 199–203.
Martin, J.H., Fitzwater, S.E., 1988. Iron deficiency limits phytoplankton growth in the northwest Pacific subarctic. Nature 331, 341–343.
Martin, J.H., Gordon, R.M., Fitzwater, S.E., 1991. The case for iron. Limnol. Oceanogr. 38, 1793–1802. Martin, J.M., Elbaz-Poulichet, F., Guieu, C., Loye-Pelot, M.D., Han, G., 1989. River versus atmospheric input
of material to the Mediterranean Sea: an overview. Mar. Chem. 28, 159–182.
McCarthy, J.J., Taylor, W.R., Taft, J.L., 1977. Nitrogenous nutrition of the plankton in the Chesapeake Bay. 1. Nutrient availability and phytoplankton preferences. Limnol. Oceanogr. 22, 996–1011.
Menzel, D.W., Spaeth, J.P., 1962. Occurrence of ammonia in Sargasso Sea waters and in rainwater at Bermuda. Limnol. Oceanogr. 7, 159–162.
Nielsen, E.S., Zhou, B., Wen Z. (translator), 1979. Photosynthesis in the Ocean. Beijing, Science Publishing House (in Chinese).
Ning, X.R., Liu, Z.L., Shi, J.X., Zhu, G.H., Gong, M., 1991. Relationship of Chl-a, bacteria, ATP, POC and respiration rate of microbe in the estuary and dilution areas of the Changjiang River (In Chinese). Acta Oceanol. Sin. 13, 831–837.
Owens, N.J.P., Galloway, J.N., Duce, R.A., 1992. Episodic nitrogen deposition to oligotrophic oceans. Nature 315, 397–399.
Pael, H.W., Rudek, J., Mallin, M.A., 1990. Stimulation of phytoplankton production in coastal waters by natural rainfall inputs: nutritional and trophic implications. Marine Biol. 119, 635–645.
Pael, H.W., Willey, J.D., Go, M., Peierls, B.L., Pinckney, J.L., Fogel, M.L., 1999. Rainfall stimulation of primary production in western Atlantic Ocean waters: roles of different nitrogen sources and co-limiting nutrients. Marine Ecol. Progr. Ser. 176, 205–214.
Paerl, H.W., 1985. Enhancement of marine primary production by nitrogen-enriched acid rain. Nature 315, 747–749.
Paerl, H.W., 1993. Emerging role of atmospheric nitrogen deposition in coastal eutrophication: biogeochemical and trophic perspectives. Can. J. Fish. Aquat. Sci. 50, 2254–2269.
Pearl, H.W., 1995. Coastal eutrophication in relation to atmospheric nitrogen deposition: current perspectives. Ophelia 41, 237–259.
Paerl, H.W., 1997. Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as ‘new’ nitrogen and other nutrient sources. Limnol. Oceanogr. 42, 1154–1165.
Paerl, H.W., Fogel, M.L., 1994. Isotopic characterization of atmospheric nitrogen inputs as sources of enhanced primary production in coastal Atlantic Ocean waters. Marine Biol. 119, 635–645.
Parsons, T.R., Maita, Y., Lalli, C.M., 1987. A Manual of Chemical and Biological Methods for Seawater Analysis, Pergamon Press, Oxford.
Peierls, B.L., Paerl, H.W., 1997. The bioavailability of atmospheric organic nitrogen deposition to coastal phytoplankton. Limnol. Oceanogr. 42, 1819–1823.
Stewart, W.D.P., 1974. Algal Physiology and Biochemistry, Blackwell, Oxford.
Thayer, G.W., 1974. Identity and regulation of nutrients limiting phytoplankton production in the shallow estuaries near Beaufort, NC. Oecologia 14, 75–92.
Willey, J.D., Cahoon, L.B., 1991. Enhancement of chlorophyll a production in Gulf Stream surface seawater by rainwater nitrate. Marine Chem. 34, 63–75.
Willey, J.D., Paerl, H.W., 1993. Enhancement of chlorophyll a production in Gulf Stream surface seawater by synthetic versus natural rain. Marine Biol. 116, 329–334.
´ ´ `
Zhang, J., 1988. Comportement geochimique des elements stables dans les grands estuaires Chinois. Ph.D. ´
Dissertation, Universite Pierre et Marie Curie.
Zhang, J., 1994. Atmospheric Wet Deposition of Nutrient Elements: Correlation with Harmful Biological Blooms in Northwest Pacific Coastal Zones. Ambio 58, 464–468.
