3 547 varied from 400 to 1167 ind / L. The horizontal distribution of microzooplankton was greater in nearshore than in offshore waters. Abundance did

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1 ACTA ECOLOGICA SINICA Vol.34 No.3 Feb DOI /stxb Ma L Cao W Q Zhang W J Lin Y S Zheng L M Yang W D Wang Y J.An ecological study on zooplankton in the northern Beibu Gulf V the effects of microzooplankton grazing on phytoplankton in summer.acta Ecologica Sinica 马璐, 曹文清 *, 张文静, 林元烧, 郑连明, 杨位迪, 王宇杰 a μ g /L d d % 66. 0% -7.4% 438.4% 8 An ecological study on zooplankton in the northern Beibu Gulf V the effects of microzooplankton grazing on phytoplankton in summer MA Lu CAO Wenqing * ZHANG Wenjing LIN Yuanshao ZHENG Lianming YANG Weidi WANG Yujie Laboratory of Marine Biology Diversity and Goble Change Collage of Marine & Earth Science Xiamen University Xiamen China Abstract In August 2011 we quantified the impact of microzooplankton grazing on phytoplankton production in the surface waters of the northern Beibu Gulf Vietnam. Shipboard dilution incubation experiments were carried out at five stations to calculate phytoplankton specific growth rates and the specific rates of grazing losses to microzooplankton. Dilution experiments using chlorophyll a Chl a as a tracer were used to estimate daily rates in two size fractions image-analyzed microscopy provided quantitative estimates of microzooplankton standing stock including ciliate and vertebrate larvae. PFW particle-free water was used to dilute seawater to five target dilutions of 0% 20% 40% 60% and 80%. Microzooplankton grazing and phytoplankton growth rates were estimated by the linear regression of AGR apparent growth rate versus dilution factor. We estimated the grazing impact of microzooplankton on phytoplankton by calculating the percentage of phytoplankton standing stock and potential primary production ingested. Average total chlorophyll a concentration was ± μg /L. Small-celled phytoplankton dominated this particular community. A notable characteristic of the phytoplankton community structure was that nano- and picoplankton made up a significant portion. Aloricate ciliates dominated the microzooplankton samples in particular Strombidium which accounted for 27.2% of total aloricate ciliate abundance. In addition loricate ciliates and copepod nauplii were recorded. Microzooplankton density * Corresponding author. wqcao@ xmu.edu.cn

2 3 547 varied from 400 to 1167 ind / L. The horizontal distribution of microzooplankton was greater in nearshore than in offshore waters. Abundance did not differ significantly with chlorophyll a concentration in this study however there was a positive correlation between microzooplankton abundance and temperature. The phytoplankton growth rate < 200 μm ranged between and 1.13 d -1 with the highest values being associated with nearshore waters. Meanwhile phytoplankton mortality due to microzooplankton grazing d -1 was highest at the same nearshore sites however growth rates were low at these sites. Consequently microzooplankton consumed 28.1% 66.0% of chlorophyll a standing stocks and -8.1% 438.4% of the primary production per day. However the grazing rate of microzooplankton on nanoplankton 2 20 μm varied from 1.87 to 0.52 d -1 with an average of 0.94±0.57 d -1. Given that the rates of grazing on phytoplankton of <200 μm were lower than those on nanoplankton we conclude that microzooplankton prefer to graze on nanoplankton. There was a positive correlation between phytoplankton growth rate and grazing rate in addition significant differences between grazing rate and chlorophyll a were found. This suggests that microzooplankton grazing activity is the main factor regulating the community structure and restraining the growth of phytoplankton. During the investigation period microzooplankton grazing effectively controlled the growth of phytoplankton consuming 176.2% of primary production on average. When grazing rates are far greater than phytoplankton growth rates energy is transferred from lower to higher trophic levels more effectively. In the surface waters of the northern Beibu Gulf microzooplankton largely control the growth of phytoplankton by grazing offshore rather than in nearshore waters where primary production is high. The growth and grazing rates combined promote planktonic ecosystem stability in this area. These results indicate that grazing by microzooplankton is a key process controlling the growth of phytoplankton in this area. Key Words microzooplankton grazing pressure phytoplankton dilution technique Beibu Gulf Microzooplankton μm HB17 HB19 HB21 HB30 HB % 70% μm 20 μm 2 μm Millpore 0.7 μm GF /F Whatman 400 ml 10 ml ml 90% 4 24 h 4-5 Turner Designs 10-AU-005-CE Chl a L Lugol's 2% 48 h 20 μm 1 5 ml μl 6

3 CA /L N V 1 V 2 CA = N V 1 /( V 2 V 3 ) V 3 Fig.1 1 Location of sampling stations in northern of Beibu Gulf 1.4 a t h AGR 200 μm μ 0.7 μm GF /F d -1 g d -1 Whatman P s 25% 50% 75% 100% P p 4 L P s = 1-e -gt 100% 10% 24 h P p = e μt -e μ-g t / e μt -q 100% 24 h ml 20 μm 0.7 μm GF /F Whatman μm Millpore a 30.6 ± 0.4 AGR = μ-g = ln P t /P 0 /t AGR μ g P o P t 31.77±

4 3 549 Station / Temperature Salinity Table 1 1 Environmental parameters at studying stations SiO - 3 / μmol /L PO - 4 / μmol /L NO - 3 / μmol /L NH + 4 / μmol /L NO - 2 achl a / μmol /L / μg /L HB HB HB HB HB SiO - 3 TIN NO - 3 NO - 2 NH + 4 TIN μmol /L 1.70±1.17 μmol /L Chl a 0.67±0.58 μg /L NO - 3 NH + 4 TIN 45.4% 1.00 μg /L 54. 3% NO - 2 TIN μg /L 2 3% PO ± Nano 2 20 μm Pico μm μmol /L 0.05 μmol / L SiO - 3 Nano Micro Pico TIN 1.69±1.35 μmol /L Chl a μmol /L Nano Chl a μmol /L μmol /L Nano Pico Pico Fig μm 2 20 μm μm Horizontal profiles of chlorophyll a for phytoplankton in the μm 2 20 μm and μm size fractions ±322 /L 17 48

550 34 1167 /L 775 /L 27. 2% 400 /L 2 16.2% 16.6% 3 565±304 /L 137±89 /L 67.1% Tintinnopsis spp. 942 /L 383 /L 56.

5 /L 775 /L 27. 2% 400 /L % 16.6% 3 565±304 /L 137±89 /L 67.1% Tintinnopsis spp. 942 /L 383 /L 56.1% 142 /L Strombidium tintinnodes 140±59 /L Taxa Table 2 2 The abundance of different group of microzooplankton in northern of Beibu Gulf Station HB17 HB19 HB21 HB30 HB32 Aloricate ciliates / /L Loricate ciliates / /L Copepod nauplii / /L Total Fig.3 3 Horizontal profiles of different group of microzooplankton in northern of Beibu Gulf 2.3 g 0.72 ± 0.46 Chl a d -1 Nano Chl a 3 4 r 2 AGR 28. 1% 66.0% -7.4% 438.4% μ 0.01±1.46 d -1 r 2

6 3 551 Table 3 Station 3 Phytoplankton growth and microzooplankton grazing rate of different size franction in northern of Beibu Gulf /μm Size-fraction μ g /d -1 /d -1 g /μ P s /% P p /% r 2 HB17 < HB19 < HB21 < HB30 < HB32 < μ g P s P p r 2 Fig.4 4 Regression of dilution experiments onboard in northern of Beibu Gulf based on total chlorophyll a a Nielsen 12 4

7 Fig.5 5 Relationship between phytoplankton standing stock growth rate with grazing rate 30 μm μm r 2 = P<0.01 μm Pico Nano 29 Gómez 17 Chl a Setala Chl a a Chl a Chl a d -1 Calbert 1 20 μm % % Calbet 1 P<0.001 r 2 = g /μ 3 g /μ> % Nano 0.11 d ±0.57 d ±0.46 d -1 Strombidium sp. Tintinnopsis sp Strombidium sp. Nano d

8 and Oceangraphy References 8 Warren A. Free-living Ciliates in the Bohai and Yellow Seas China / /Song W B Hu X K Trans. Beijing Science Press Xu D P Song W B. Tintinnid ciliates from qingdao Protozoa Ciliophora Tintinnida. Acta Zootaxonomica Sincia Landry M R Hassett R P. Estimating the grazing impact of marine micro-zooplankton. Marine Biology Burkill P H Head E Fransz G. Grazing by microzooplankton / / SCOR /JGOFS Report No. 6 Coremeasurement protocols. Reports of the Core Measurement Working Groups Nielsen T G Ki rboe T. Regulation of zooplankton biomass and production in a temperate coastal ecosystem. 2. Ciliate. Limnology 13 Suzanne L S Erin L M Olson M B. Microzooplankton grazing in the coastal gulf of Alaska variations in top-down control of phytoplankton. Limnology and Oceanography Zhang C X Zhang W C Zhao N Xiao T. Distribution of planktonic ciliates in autumn and winter in the shelf areas of the East China Sea. Acta Oceanologica Sinica Archer S D Leakey R J G Burkll P H Sieigh M A. Microbial 1 Calbet A Landry M R. Phytoplankton growth microzooplankton dynamics in coastal waters of east Antarctica herbivory by grazing and carbon cycling in marine systems. Limnology and Oceanography heterotrophic dinoflagellates Marine Ecology Progress Series 2 Stelfox C E Burkill P H Edwards E S Harrisa R P Sleighb M A. The structure of zooplankton communities in the 2 to 2000 μm size range in the Arabian Sea during and after the SW monsoon 16 Rose J M Caron D A. Does low temperature constrain the growth rates of heterotrophic protists Evidence and implications for algal blooms in cold waters. Limnology and Oceanography Deep Sea Research Part II Topical Studies in Oceanography / Suzuki K Tsuda A Kiyosawa H Takeda S Nishioka J Saino T Takahashi M Wong C S. Grazing impact of microzooplankton on a diatom bloom in a mesocosm as estimated by pigment-specific dilution technique. Journal of Experimental Marine Biology and Ecology Ma R Y Li J Zheng E W Huang S F. ENSO makes an impact on the storm tide of Guangxi coasting area around the Beibu Gulf. Journal of Guangxi University Natural Science Edition Gómez F. Trends on the distribution of ciliates in the open Pacific Ocean. Acta Oecologica Set l O Kivi K. Planktonic ciliates in the Baltic Sea in summer distribution species association and estimated grazing impact. Aquatic Microbial Ecology Zhang C X Zhang W C Xiao T. Ciliate abundance and biomass in northern South China Sea in October Acta Ecologica Sinica Quevedo M Viesca L Andón R Fernández E. The protistan microzooplankton community in the oligotrophicnorth-eastern 5 Cheng Q Y Li F H. The marine environmental protection Atlantic large-and mesoscale patterns. Journal of Plankton condition and strategy in Guangxi's littoral. Environmental Science and Management Sun J Song X X Yin K D Liu D Y. Preliminary study of Research Zeng X B Huang B Q. Grazing impact of microzooplankton in Taiwan strait and its contribution to nutrient regeneration. Journal microzooplankton herbivory in Hong Kong in summer. Acta of Xiamen University Natural Science Ecologica Sinica Sun J Feng Y Y Zhang Y H Hutchins D A. Fast 7 Xu K D Hong H S Song W B Ke L Ma H G. Studies on microzooplankton grazing on fast-growing low-biomass tintinnine ciliates in the Taiwan strait Ciliophora Tintinnina. Acta Zootaxonomica Sinica phytoplankton A case study in spring in Chesapeake Bay Delaware Inland Bays and Delaware Bay. Hydrobiology Zhang J T Yin K D Dong L H. Microzooplankton grazing rate of size-fractionated phytoplankton in spring in the Yellow Sea China. Marine Sciences Sun J Dawson J Liu D Y. Microzooplankton grazing on phytoplankton in summer in the Jiaozhou Bay China. Chinese

9 Journal of Applied Ecology Huang B Q Xiang W G Zeng X B Chiang K P Tian H J Hu J Lan W L Hong H S. Phytoplankton growth and microzooplankton grazing in a subtropical coastal upwelling system in the Taiwan Strait. Continental Shelf Research S38-S Dupuy C Talarmin A Hartmann H J Delmas D Courties C Marquis E. Community structure and grazing of the nanomicrozooplankton on the continents shelf of the Bay of Biscay. Estuarine Coastal and Shelf Science Ichinotsuka D Ueno H Nakano S. Relative importance of nanoflagellates and ciliates as consumers of bacteria in a coastal sea area domainated by oligotrichous Strombidium and Stobilidium. Aquatic Microbial Ecology Gifford D J. Impact of grazing by microzooplankton in the Northwest Arm of Harlifax Harbour Nova Scotia. Marine Ecology Progress Series ENSO Warren A. / / Dawson J

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