PLEASE SCROLL DOWN FOR ARTICLE

This article was downloaded by: [Academia Sinica]On: 23 March 2011Access details: Access Details: [subscription number 933922605]Publisher Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Journal of Freshwater EcologyPublication details, including instructions for authors and subscription information:http://www.informaworld.com/smpp/title~content=t925992003

The Picophytoplankton in Three Chinese Lakes of Different Trophic Statusand Its Relationship to Fish PopulationsJian Wang; Ping Xie; Noriko Takamura; Liqiang Xie; Zaojun Shao; Huijuan Tang

Online publication date: 07 January 2011

To cite this Article Wang, Jian , Xie, Ping , Takamura, Noriko , Xie, Liqiang , Shao, Zaojun and Tang, Huijuan(2004) 'ThePicophytoplankton in Three Chinese Lakes of Different Trophic Status and Its Relationship to Fish Populations', Journalof Freshwater Ecology, 19: 2, 285 — 293To link to this Article: DOI: 10.1080/02705060.2004.9664543URL: http://dx.doi.org/10.1080/02705060.2004.9664543

Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf

This article may be used for research, teaching and private study purposes. Any substantial orsystematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply ordistribution in any form to anyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss,actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directlyor indirectly in connection with or arising out of the use of this material.

The Picophytoplankton in Three Chinese Lakes of Different Trophic Status and Its Relationship to Fish Populations

Jian Wanga, Ping Xieasb, Noriko Takamurac, Liqiang Xiea, Zaojun Shaoa, and Huijuan Tanga

ABSTRACT

A year-round comparison was made of the picophytoplankton populations in three lakes of different trophic status (oligotrophic, mesotro- phic, and hypereutrophic), as well as in experimental enclosures stocked with various densities of fish. Picophytoplankton abundance was significantly different between the hypereutrophic lake and the oligotrophic lake (P<0.018) and between the hypereutrophic lake and the mesotrophic lake (P<0.021), whereas the difference between the mesotrophic and oligotrophic lakes was not significant (P<0.745). The effect of total nitrogen:total phosphorus ratio on the abundance of picophytoplankton was demonstrated in the oligotrophic lake, but such effect did not manifest itself in the other lakes or in the experimental enclosures. The average annual picophytoplankton population sizes in the three lakes in 1995 -1998 were correlated with estimated fish abundance (r=0.824, n=9, P=0.006). The results of enclosure experiments demonstrated that the abundance of picophytoplankton increased with the stocking density of fish (r=0.619, n=8. P=0.100).

INTRODUCTION

Picophytoplankton is a principal component of freshwater communi- ties; its dynamics are important to the understanding of the structure and function of freshwater ecosystems, especially with respect to material cycling (Callieri et al. 2002). Initial estimates show that picophytoplankton abun- dance decreased in waters of greater nutrient content (Stockner and Antia 1986). There have been a large number of investigations on picophytoplankton distribution (Sondergaard 1990, Fahnenstiel and Carrick 1992) and on contributions to total phytoplankton biomass and primary production in lakes (Voros et al. 199 1, Takamura and Yukihiro 1994, Carrick and Schelske 1997, Nechama et al. 1997). Some studies showed that the picophytoplankton is an important contributor to total phytoplankton biomass and primary production and apparently decreases in importance with increasing nutrient levels (Craig 1984, Fahnenstiel et al. 1986, Stockner 1987. Stockner and Shortreed 1991).

Another study showed that the picophytoplankton contributions to total phytoplankton biomass and primary production were lower in an oligotrophic lake (Nechama et al. 1997) and of increasing importance with increashg nutrients in eutrophic and hypereutrophic lakes (Cronberg and Weibull 198 1, Bailey and Komarek 199 1, Takamura et al. 1992, Carrick and Schelske 1997, Wang and Lin 1998).

Since 1986, Cyanophyta blooms were replaced by small-sized species of algae in Lake Donghu of China (Wang and Liu 1991). and diminution in the size of algae has been a problem in this lake. Currently, there is an urgent need for an increased understanding of the function of picophytoplanlcton in

a Donghu Experimental Station of Lake Ecosystems, State Key Laboratory for Freshwater Ecology and Biotechnology of China, Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan 430072, P.R China. Author to whom correspondence should be sent (E-mail: xieping@ihb.ac.cn) National Institute for Environmental Studies. Tsukuba, Ibaraki. 305 Japan.

Journal of Freshwater Ecology, Volume 19, Number 2 - June 2004

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

this aquatic ecosystem. Previous work on picophytoplankton of Lake Donghu was limited and focused on abundance, biomass, and production (Wang and Lin 1998). and there are few comparative studies on waters of difTerent trophic status (Takarnura and Yukihirol994. Carrick and Schelske 1997). The present study aimed to describe picophytoplankton distribution and the effects of total nitrogen (TN):total phosphorus (TP) on picophytoplankton abundance in three lakes with different trophic status, and to analyze the possible effects of the fishery on the picophytoplankton.

MATERIALS AND METHODS

Lake Dongting is a large oligotrophic lake that is connected directly to the Yangtze River. We sampled this lake at five stations near the Yangtze River. Lake Bao'an is mesotrophic with an extensive macrophyte community. We sampled at three different stations in this lake. Lake Donghu is a hypereutrophic lake with a high annual nutrient input. We sampled this lake at four stations. Morphometric and hydrobiologic data for these lakes are shown in Table 1. In recent decades, the four domestic Chinese carp (silver carp, bighead carp, grass carp, and black carp) have been intensively stocked in Lake Donghu and Lake Bao'an. while no stocking has been done in Lake Dongting.

Table 1. Physical and chemical data for the three study lakes. Lake Donghu Bao'an Dongting

Location E l 14°23'N30033

Lake area (km2) 32.0 Max depth (m) 4.7

Mean depth (m) 2.2

Water Temp (OC) 4.2-32. Secchi(cm) 40- 160 Chl a (pg 1-1) 0.89-196

TN( mg 1-1) 0.765-9.9991 TP (mg 1-1) 0.029-0.4997

DOC (p mol. 1.') 14.3 POC/ Clll a 52.78

Our sampling program was carried out monthly during 1995 - 1998 in Lake Donghu, bimonthly during 1996 - 1997 in Lake Dongting, and bimonthly during 1996 - 1998 in Lake Bao'an. Data from 1996- 1997 were used for year- round comparisons of the picoplankton populations with the Newrnan-Keuls test. Samples were collected 0.5 m below the surface and 0.5 m above the bottom with a 2.5 1 modified Patalas bottle sampler, mixed, and fixed with formaldehyde. Subsamples for picophytoplankton counting were filtered through 0.2 pm pore-size Nucleopore filters under gentle vacuum. Phytoplank- ton of >2.0 pm size was counted after sedimentation of one liter of lake water for 48 h.

Picophytoplankton on the Nucleopore filters was enumerated by an Opton fluorescence microscope (PLAN-NEOFLUAR 100X. BP450-490, FT510, LP520) at magnification of 1000 x to 1250 x using a 100 x objective, and at least 300 cells in each filter were counted, corresponding to 10-50 random fields of vision. Direct microscopic counting of quantitative samples of >2.0 pm phytoplankton was conducted using a 0. I'm1 counting chamber at a

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

magnification of 400 x, and the abundance and cell volume of each phyto- plankton species were estimated. Biomass was calculated from cell volume (including picophytoplankton) assuming a cell density of 1 mg mrn-3.

Samples for chlorophyll a were filtered through Whatman GF/C filters and extracted for 24 hours in 90% ethanol. Chl a was measured spectrophotometrically and corrected for phaeophytin according to Lorenzen (1967). From one liter samples, rotifers were examined using 1 ml subsamples (Shao et al. 20011.

Determination of TN and TP was after digestion with alkaline potassium persulfate at 1200C for 30 min. TN was measured as nitrate and absorption was measured at 220 nm. Total phosphorus was analyzed with the ammonium molybdate method after digestion with H2SO4 (Qian and Fu 1987). The transparency and temperature were determined at the time of sampling.

Fish yields of the three lakes were obtained from fish catches registered at the local fish farm or from unpublished survey data of G.T. Huang, Institute of Hydrobiology, Chinese Academy of Sciences. We assessed the relationship between the fish yield and picophytoplankton abundance in the three lakes, and we also examined this relationship with an enclosure experiment.

The enclosure experiment was conducted during spring and summer of 1999 in the littoral zone of Lake Donghu. Eight enclosures (2.5 x 2.5 m and 3.0 m deep). made of polyhexene with nylon reinforcement, were hung from steel pipes. The enclosures were close to the sediment in order to prevent fish escape: they were filled with lake water to a depth of 2.5 m. Sediment (about 10 cm) from the lake was added into each enclosure several days before the fish stocking. The planktivorous filter-feeding silver carp was used in the experiment.-silver carp from a hatchery were acclimated in a net cage in the lake for three days before being put into the enclosures. Four fish densities (each with two replicates) were-established. The stocking levels of silver carp were 0, 116, 190, and 340 g m-2 silver carp. Mean individual weight and length of stocked silver carp were 108.5 (256.1 g) and 23.2 (24.4 cm). Enclosures were sampled once a week. Two lake stations nearby the enclosures were also sampled.

RESULTS

Annual mean abundance of picophytoplankton ranged from 0.19 x 104 ind.ml-1 in Lake Dongting to 7.65 x 104 ind.ml-1 in Lake Donghu (Fig. 1). There - -

were significant differences between Lake Donghu and Lake ~ongt ing (P<0.018), and between Lake Donghu and l&e Bao'an (P<0.021). There was no significant difference between Lake Dongting and Lake Bao'an (P<0.745). The greatest abundance of picophytoplankton usually occurred during June and July every year.

The abundance of picoplankton was positively correlated with TN:TP ratio in the oligotrophic lake (r=0.543,P=0.002), but no significant correlations were found in the mesotrophic (r=0.309. P=0.2) or hypereutrophic lakes (r=- 0.088. P=0.84) (Fig.2). In the enclosure experiment, nutrient levels and picophytoplankton abundance were not correlated (Fig.3).

Picophytoplankton showed an increase with increased fish yield (r=0.824. P=0.006; Fig. 4).

Total picoph~oplankton biomass was significantly higher in the enclosures with high fish density than in those with low fish density (Fig.5). and this represented 20% of the total phytoplankton biomass. There was a positive relationship between the abundance of picophytoplankton and stocking density of fish (r=0.619. n=8. P=O. 100)(Fig.6), but the

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

8 Lake Donghu r, I

6 Lake Bao'an

z 5 d .5 4

2 3 - 2

1

0

I 11 111 IV I 11 111 1 11 I11 IV V

S t a t i o n s

Figure 1. Annual mean abundance of picophytoplankton in three lakes.

-10 0 10 20 30 40 50 80 70 80 90

TN TP rabo

Figure 2. Relationship between picophyt ratio in lakes and enclosures.

90 : ; : : : : : : : :

220 - -- 200 E leu

e 180 Enclosure n=64 r=O 04963 p>O 05

80

*$ 70

-20 1 I 0 5 10 15 20 25 30 35 40 45

TN TP ratlo

:oplankton abundance and the TN:TP

. , . . . , , , , , ; . ; ; ; ; ; ; ; : j Lake Donghu I=-0.M. n=78. p>0.05

TP(mg 1') TP (mg.ll)

Figure 3. Relationship between picophytoplankton and total phosphorus in (a) enclosures and in (b) lakes.

- 6 0 i i . ; i ; ; i ; j j . , . . . , , . , . . , . , . . . . , . - . : : . ; j ; : : : : : . , , . , . , . 6 4 0 i i : : ; I I : ; ;

$ , o ; i o i : : : : : : : : : * ; i i i i i . , , , , . , . .

, . . , b : : . , . . ! . - I

. . ,

n o . . . -0.j.. ; b ; ;- , . . . . , , . , , -10 " " " " "

-10 0 10 20 30 40 50 80 -20 0 20 40 80 80 1M 120 140 150 180 200

TN'TP RUO TN:TP ratlo

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

8

7

c 6 3 -7 5 z - u 4 8 r 2% 3 '=;; 2 8 - , a

0

-1 100 200 300 400 500 600 700 800 900 lo00

annual fish y~eld (kg haS')

Figure 4. Relationship between picophytoplankton abundance and annual fish yield in lakes (r=0.824; n=9; P=0.006).

100%

mJll qnrophyta 80%

a Cyanophyta 60% Chlorophyta 0 C r y ~ t ~ ~ h y t a 40%

Euglenophyta 20% % Picophytoplankton 0 Bacilariophyta 0%

29lA 6 M 13M 20M 2 7 M 311 911 2111 26/J

Figure 5. Biomass distribution of phytoplankton in the enclosures and the surrounding lake water. Values are means of two replicate enclosures (NF= no fish, LF= 116 g m-2, MF= 190 g m-2, HF=340 g m-2).

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

picophytoplankton biomass, as a percentage of total phytoplankton, was reduced. All the enclosures were dominated by Cryptophyta species. The abundances of Cyanophyta and picophytoplankton were significantly lower in the fish-free enclosures than in all other enclosures, while the Englenophyta abundance tended to be higher. Rotifer abundance was reduced in the presence of silver carp (Fig. 7); Polyarthra vulgaris and Brachionus spp. dominated in the fish-free enclosures, and their abundances were notably reduced in the presence of fish.

Fish weight (g.mZ)

Figure 6. Relationship between the density of picophytoplankton and the abundance of stocked silver carp in the enclosures (r=0.619, n=8, P=O. 100).

DISCUSSION

Experiments on the role of planktivorous fishes in the elimination of Microcystis spp. blooms have been conducted with enclosure methods. The algal blooms that appeared in the fish-free enclosures were completely eliminated in 10-20 days by introduction of silver and/or bighead carp (Xie and Liu 2001). In our enclosure experiments, although the picophytoplankton abundance increased with increased fish stocking, the biomass of picophytoplankton relative to total phytoplankton decreased. We demonstrated that fish stocking exerted effects not only on picophytoplankton but also on >2.0 prn phytoplankton. In Hungarian shallow lakes, high picophytoplankton cell densities were observed in eutrophic to hypereutrophic waters, but the contribution of picophytoplankton to overall phytoplankton biomass and production was relatively low (Voros et al. 1991). Our studies showed clearly that grazing pressure by planktivorous fishes is a key factor in shaping the size of algae and picophytoplankton that are dominant in a lake.

Fish stocking exerted a greater influence on picophytoplankton abundance than nutrients. In our enclosure experiment, high nutrient concentration was not accompanied by high picophytoplankton density. Stockner and Shortreed (1991) suggested that average picophytoplankton abundance is positively related to average TP content of lake water at TP concentration <60 mg m-3. In our study, since TP concentration in the lakes or enclosures was usually over 60 mg m-3, phosphorus was not a limiting factor. However, phytoplankton density was related closely to the ratio of TN/TP in the oligotrophic Lake Dongting. It is reported that small phytoplankton (<2 pm) may not be as susceptible to severe P limitation as larger-sized phyto- plankton and that low P concentrations favored the predominance of algal picoplankton (Wehr 1989 and 19911. It remains unknown whether picophyto- plankton can out-compete large phytoplankton for phosphorus. Wehr (1991) reported that picophytoplankton was relatively abundant when phosphorus

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

was limiting and nitrogen was in surplus. Picophytoplankton may often be N-limited, although some species are able to f k atmospheric nitrogen (Mitsui et al. 1986, Phlips et al. 1989).

In our enclosure experiment, Cyanophyta and picophytoplankton were rare in the fish-free enclosures probably because of grazing pressure by zooplankton. while Euglenophyta, Chlorophyta and Polyarthra vulgaris were abundant. The results indicate that silver carp at high densities may shift both the competitors and predators of picophytoplankton. Rotifers are important grazers of picophytoplankton in fresh waters (Caron et al. 1985, Stockner 1987). and it may be that Protozoa also control the variations of picophytoplankton (Pernthaler et al. 1996, Callieri et al.. 2002). However, no data were available for ciliates or heterotrophic nanoflagellates here. It may be concluded that in eutrophic waters, filter-feeding silver carp at high density depress picophytoplankton predators such as rotifers, and thus allows picophytoplankton to increase.

Figure 7. Changes of rotifer abundance in the presence of silver carp stocked at different densities. NF=no fish, LF= 1 16 g m-2, MF= 190 g m-2, HF=340 g m-2).

ACKNOWLEDGEMENTS

The authors thank all the menlbers of the Donghu Experimental Station of Lake Ecosystems, CLKN, for their assistance in the field and laboratory work. This work was supported by the Key Project of CAS (Grant No KZCX1-SW- 12) and the Project of National Natural Science Foundation of China (No.39970 13 1).

LITERATURE CITED

Bailey-Watts. A.E. and J. Komarek. 1991. Towards a formal description of a new species of Synechomccus (Cyanobacteria/Cyanophyceae) from the freshwater picoplankton. Arch. Hydrobiol. (suppl). 88:5- 19.

Callieri, C., S.M. Karjalainen, and S. Passoni. 2002. Grazing by ciliates and heterotrophic nanoflagellates on picocyanobacteria in Lago Maggiore, Italy. J. Plankton Research 24: 785-796.

Caron. D. A., F.R. Pick, and D.R.S. Lean. 1985. Chroococcoid cyanobacteria in Lake Ontario: vertical and seasonal distributions during 1982. J. Phycol. 21: 171-175.

Carrick H.J. and C.L. Schelske. 1997. Have we overlooked the importance of small phytoplankton in productive water? Limnol. Oceanogr. 42: 16 13- 1621.

Craig. S.R. 1984. Productivity of algal picoplankton in a small meromictic lake. Int. Ver. Limnol. Verhandl. 22: 35 1-354.

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

Cronberg, G. and C. Weibull. 198 1. Cyanodictyon imperfecturn a new chroococcal blue-green alga from Lake Trurnrnen,Sweden. Arch. Hydrobiol. (suppl). 60: 101 - 1 10.

Fahnenstiel G.L. and H.J. Carrick. 1992. Phototrophic picoplankton in Lakes Huron and Michigan: abundance, distribution, composition and contribution to biomass and production. Can. J. Fish. Aquat. Sci. 49: 379-388.

Fahnenstiel, G.L.. L. Sicko-Goad, D. Scavia, and E.F. Stoermer. 1986. Importance of picoplankton in Lake Superior. Can. J. Fish. Aquat. Sci. 43: 235-240.

Lorezen, C.J. 1967. Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol. Oceanogr. 12: 343-346.

Mitsui, A.S., A. Kumazawa. H. Takahashi, S.C. Ikemoto, and T. Arai. 1986. Strategy by which nitrogen-fudng cyanobacteria grow photoautotrophically. Nature 323: 720-722.

Necharna, 2.. M. Rushanky. T. Berman, and Z. Dubinsky. 1997. Seasonal photosynthetic activity of autotrophic picoplankton in Lake K i ~ e r e t , Israel. J. Plankton Res. 19: 979-993.

Pernthaler, J . , K. Sirnek, B. Sattler, A. Schwarzenbacher, J . Bobkova, and R. Psenner. 1996. Short-term changes of protozoan control on autotrophic picoplankton in an oligo-mesotrophic lake. J . Plankton Res. 18: 443- 462.

Phlips, E.J., C. Zeman, and P. Hansen. 1989. Growth, photosynthesis, nitrogen fixation and carbohydrate production by a unicellular cyanobacterium, Synechococcus sp. (Cyanophyta) . J. Appl. Phycol. 1 : 137-145.

Qian. J.N. and L.M. Fu. 1987. Simultaneous determination of total nitrogen and total phosphorus in water using peroxodisulfate oxidation. Environ. Sci. 8: 8 1-84 (in Chinese).

Shao. Z.J.. P. Xie, and Y. Zhuge. 2001. Long-term changes of planktonic rotifers in a subtropical Chinese lake dominated by filter-feeding fishes. Freshwater Biol. 46: 973-986.

Sondergaard, M. 1990. Picophytoplankton in Danish Lakes. Verh. Int. Ver. Limnol. 24: 609-612.

Stockner, J.G. 1987. Lake fertilization: the enrichment cycle and lake sockeye salmon (Oncorhynchys nerka) production. Can. Spec. Publ. Fish. Aquat. Sci. 96: 198-215.

Stockner. J.G. and N.J. Antia. 1986. Algal picoplankton from marine and freshwater ecosystems: a multidisplinary perspective. Can. J . Fish. Aquat. Sci. 43: 2471-2503.

Stockner. J.G. and K.S. Shortreed. 199 1. Autotrophic picoplankton: commun- ity composition, abundance and distribution across a gradient of oligotrophic British Columbia and Yukon Territory lakes. Int. Rev. Ges. Hydrobiol. 76: 58 1-60 1.

Takarnura, N. and N. Yukihiro. 1994. Picophytoplankton biomass in relation to lake trophic state and the TN:TP ratio of lake water in Japan. J. Phycol. 30: 439-444.

Takamura, N., X.B. Zhu, H. Q. Yang. L. Ye. F. Hong, and T. Miura. 1992. High biomass and production of picoplankton in a Chinese integrated fish culture pond. Hydrobiologia 237: 15-23.

Voros, L., P. Gulas, and J. Nemeth. 1991. Occurrence, dynamics and production of picoplankton in Hungarian shallow lakes. Int. Rev. Ges. Hydrobiol. 76: 6 17-629.

Wang. J. and W.L. Lin. 1998. Ecological approaches of algal picoplankton in Donghu Lake. J. Lake Sci. 10: 76-8 (in Chinese with English abstract).

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011

Wang. J. and J.K. Liu. 1991. Role of phosphorus cycling in algal metabolism and algal succession in Lake Donghu, China. Arch. Hydrobiol. 120: 433-445.

Wehr, J.D. 1989. Experimental tests of nutrient limitation in freshwater picoplankton. Appl. Environ. Microbial. 55: 1605- 16 1 1.

Wehr. J.D. 1991. Nutrient and grazer-mediated effects on picoplankton and size structure in phytoplankton communities. Int. Rev. Ges. Hydrobiol. 76: 643-656.

Xie, P. and J.K. Liu. 2001. Practical success of biomanipulation using filter- feeding fish to control cyanobacteria blooms: a synthesis of decades of research and application in a subtropical hypereutrophic lake. Sci. World J. 1: 337-356.

Received: 14 October 2003 Accepted: 1 February 2004

Downloaded By: [Academia Sinica] At: 02:34 23 March 2011