Seasonal variation in zooplankton composition and grazing impact on phytoplankton standing stock in the Pearl River Estuary, China

ARTICLE IN PRESS

Continental Shelf Research 24 (2004) 1949–1968 www.elsevier.com/locate/csr

Seasonal variation in zooplankton composition and grazing impact on phytoplankton standing stock in the Pearl River Estuary, China Yehui Tan, Liangmin Huang, Qingchao Chen, Xiaoping Huang South China Sea Oceanography Institute, Chinese Academy of Sciences, Guangzhou, China Received 12 December 2002; accepted 25 April 2004 Available online 1 September 2004

Abstract The composition, abundance, distribution and grazing impact of dominant components of the meso- and macrozooplankton community were investigated in the Pearl River Estuary (PRE) wet and dry season cruises during the summer of 1999 and winter 2000, respectively. Throughout the investigation, mesozooplankton, comprised mainly of copepods, dominated numerically and by species richness, accounting for at least 73% of the total mesozooplankton in the PRE. The copepods Acartia spinicauda, Pavocalanus crassirostris, Oithona rigida, Paracalanus aculeatus and Euterpina acutifrons, numerically dominated zooplankton counts, while during the dry season the zooplankton community was dominated by the copepods Paracalanus serrulus, Pavocalanus crassirostris, Paracalanus parvus, Acartia spinicauda and Oithona spp. The average evacuation rates of the copepods were 0.03270.006 and 0.03970.008 min
1 for winter and summer, respectively. The grazing impact of the most abundant zooplankton taxa accounted for up to 85% of all zooplankton counted at each station. The grazing impact of zooplankton, especially copepods, changed seasonally and spatially, varying between o0.3% and 75% of the chlorophyll standing stock, or up to 104% of the daily phytoplankton production in summer and 21% in winter. r 2004 Elsevier Ltd. All rights reserved. Keywords: Mesozooplankton; Copepods; Grazing; Pearl river estuary; Gut fluorescence

1. Introduction The Pearl River Estuary (PRE) is created by the flow of freshwater from the largest river system in southern China into the South China Sea, and the Corresponding author

E-mail address: [email protected] (Y. Tan).

estuary is characterized by strong vertical gradients (salinity, turbidity and nutrients) which leads to varying environmental conditions for estuarine organisms. Nutrient enrichment in the PRE resulting from municipal and livestock waste discharges has been a major environmental concern over the past two decades. Eutrophication indicated by phytoplankton blooms in the upper

0278-4343/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.csr.2004.06.018

ARTICLE IN PRESS 1950

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

reaches of the estuary in recent years has induced frequent algal blooms and red tides in Guangdong and Hong Kong coastal waters (Holmes and Lam, 1985). There has been considerable debate about the role of zooplankton in controlling algal blooms through grazing (Harris and Malej, 1986; Peter, 2001). Grazing by the copepod community is also important during the initial stage of algal blooms (Uye, 1986), and can cause a shift in phytoplankton species composition and modify the food web structure (Bathmann et al., 1990). Many studies have pointed to the significance of the trophic relationship between phytoplankton and zooplankton in estuarine ecosystems (Sautour et al., 1996). An increase in nutrient loading can cause an increase in phytoplankton productivity and standing stocks (Breitburg et al., 1999), especially in the large-sized phytoplankton (Kilham and Kilham, 1984). These changes may in turn result in an increase in copepod feeding and ingestion. Several previous studies have indicated that large phytoplankton cells are more likely to be ingested by mesozooplankton that are dominated by copepods (Uye, 1986; Bautista and Harris, 1992; Nejstgaard et al., 1995; Hansen et al., 2000). In addition, increased nutrient loadings may cause a change in the ratio of macronutrients that may alter zooplankton species composition, dominance and succession (Breitburg et al., 1999; Park and Marshall, 2000). In freshwater systems, the total zooplankton abundance may increase with increasing eutrophication, while large species may be replaced by small species (Beaver and Crisman, 1982; Bays and Crisman, 1983; Pace, 1986). The response of the copepod community structure to eutrophication has not yet been well documented in estuarine ecosystems. Several previous studies have been conducted on the chemical and physical control of harmful algal blooms in the PRE (Zhang and Dickman, 1999), but the contribution of zooplankton grazing to the decline of phytoplankton blooms and the role of copepod grazing in controlling the estuarine food web structure remain essentially unknown in this region. Thus, understanding the grazing impact on phytoplankton standing stocks and the extent to which zooplankton grazing is affected by the

phytoplankton assemblage may provide insights into the mechanisms of the dynamics of algal blooms in the PRE. During our study, a survey of the zooplankton species composition and feeding activity was carried out in two seasons (summer and winter) and from the inner to the outer part of PRE. We examined the zooplankton population dynamics in the PRE during the summer of 1999 and winter 2000. We attempted to relate the gut evacuation rates to estimate the grazing impact on phytoplankton blooms or red tides in the PRE.

2. Materials and methods The two cruises were carried out one, during the wet season, between July 14 and 28, 1999, and the second cruise from January 7 to 10 in the dry season. Sampling stations, including three anchored 24 h stations (C1, C2 and C3) in the wet season, in the PRE are shown in Fig. 1. The temperature, salinity, light penetration and current speed were obtained by using a YSI6820 Water Quality System. 2.1. Zooplankton taxonomic composition, abundance and biomass Zooplankton taxonomic composition and abundance were investigated at 31 stations and three anchored stations during the wet season and at 21 stations during the dry season. A zooplankton net (50 cm diameter, length 208 cm, 169 mm mesh) with a flow meter was towed vertically from 1.5 m above the seabed to the surface. At the three anchored stations, samples were collected approximately every 3 h for a total of 26 h (sampled 8 times a day). Due to vertical stratification, a closing net was used to obtain separate samples above and below the salinity transition layer, based on ADCP results. The zooplankton samples were rinsed and preserved in 5% formalin for further identification of species and enumeration in the laboratory. The Shannon-Wiener diversity index (H0 ) (Ma, 1994) and Pielou’s Evenness Index (J) (Pielou, 1966) for zooplankton was calculated

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

22.7

1951

1 2

22.6

12

3 4 6 7 5 C1

22.5

8 9 11 18

30 Hong Kong

22.4 C3 22.3

13

10

14 15

17

29

16 C2

Lantau Is

19

22.2

28 26

20

22.1

27

25 24

22

23 22

21.9

21 31 113.4

113.5

113.6

113.7

113.8

113.9

114

114.1

114.2

114.3

114.4

114.5

Fig. 1. Sampling stations in the PRE.

according to the following equation: H0 ¼


s X

Pi ln Pi ;

i¼1

J ¼ H 0 =Hmax ¼ H 0 =ln S; where Pi is the proportion of species i in the samples and S is the species richness. 2.2. Gut pigment content Gut pigments of the copepods were analyzed at 31 stations and three anchored stations (C1, C2, C3) during the wet season and at 21 stations during the dry season. All stations were sampled at least twice during the same time period from 07.00 to 12.00. The gut fluorescence method was used to estimate the ingestion of phytoplankton by the calanoid copepods. Animals collected from the first net tow were preserved in 5% formaldehyde for species identification. Animals collected in the second and third net tows were immediately frozen in liquid nitrogen and stored in a freezer for

measurement of gut pigment content in the laboratory. In the laboratory, 30–50 adult females or IV–V copepodites of the listed species with the highest abundance were examined to estimate the copepod gut contents since most of the adult males do not feed (Mauchline, 1998). Individuals of Acartia spinicauda, Pavocalanus crassirostris, Oithona rigida and Paracalanus aculeatus in the wet season, and Paracalanus serrulus, Pavocalanus crassirostris, Subeucalanus subcrassus, Temora turbinata, Bestiola sinicus, Acartia spinicauda and Calanus sinicus were sorted rapidly from each sample in the dry season, rinsed with filtered seawater, transferred to small glass tubes containing 10 ml of 90% analytical acetone and extracted for 24 h. Fluorescence of the acetone extracts before and after acidification with one drop of 10% HCl was measured with a Turner Designs 10-AU-005-CE fluorometer. The average gut content of the copepods was calculated using the equations of Mackas and Bohrer (1976), and were expressed as ng Chl a per individual copepod. Gut evacuation rates (k, min
1) were then derived from

ARTICLE IN PRESS 1952

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

the slope of regression of the natural logarithm of gut pigment versus time. At stations where gut evacuation values were not available, the average value for each species was employed for those stations. In order to estimate the community grazing impact, copepod abundance data were multiplied with the individual ingestion rates. To convert Chl a concentrations into carbon, an average Chl a: carbon ratio of 50 was employed (Atkinson et al., 1996). The grazing impact was then expressed as the percent integrated phytoplankton standing stock and percent daily primary production consumed per day. 2.3. In situ gut evacuation experiments Gut evacuation experiments were conducted at the three anchored stations (C1, C2 and C3) during the wet season at 16.00. At station C2, experiments were conducted 8 times (3 h intervals during the 24 h period) and also at stations 5, 10 and 19 at 16:00 during the dry season. After collection, the copepods were gently rinsed with seawater on a 200 mm mesh and transferred to a small bucket with a 125 mm mesh on the bottom. The bucket was then placed in a big bucket containing 25 l of filtered seawater (0.45 mm), at the ambient surface water temperature and salinity. At various time intervals (every few minutes for a total of 1 h), a subsample of copepods was taken and immediately frozen in liquid nitrogen. The gut pigment content was analyzed in the laboratory as described above. Gut evacuation rates were only analyzed for female herbivorous copepods because adult males of many species do not feed. The decline in gut pigment content over time was modeled as an exponential function and can be described by the following equation: G t ¼ G 0 e
kt ; where G 0 is the initial gut pigment content per individual, G t is the gut content at time t and k is the rate constant of the gut evacuation (min
1). The ingestion rate (I, ng ind
1 h
1) was calculated as I ¼ k  G;

where G (ng ind
1) is the average gut pigment content of two distinctive feeding periods (Morales et al., 1993). The grazing impact by the copepods (T, %) was calculated as described by Morales and Harris (1990): T ¼ A  I=C; where A (ind m
3) is the zooplankton abundance. We used an estimate of 67% as the ratio of herbivore zooplankton to total abundance. C (mg m
3) is the concentration of chlorophyll a in the water column. Gut pigment values were corrected for pigment destruction during gut passage using an estimated average loss of 33% (Kiørboe and Tiselius, 1987; Dam and Peterson, 1988; Atkinson et al., 1996). 2.4. Chl a and primary productivity Water samples for Chl a were pre-filtered through a 200 mm screen to remove larger zooplankton. Subsamples of 100 ml that corresponded to the sampling depth were filtered through 0.45 mm membrane filters with a vacuum of o100 mmHg to collect Chl a. Filters were kept frozen at –20 1C and extracted with acetone and in vitro fluorescence was determined with a Turner Designs Fluorometer Model-10 AU as described above. Water samples for primary productivity were collected before noon at 100%, 50%, 30% and 1% of the surface irradiance and pre-filtered through a 200 mm screen to remove larger zooplankton. Duplicate 50 ml samples were incubated with 1or 2 mCi 14C-labeled sodium bicarbonate in direct sunlight and neutral density screens were used to simulate the light intensity from which the samples were collected. The temperature in the on-deck incubators was regulated by flowing surface seawater. Dark bottles were incubated simultaneously under the same conditions. All of samples were incubated for about 4 h. The incubations with 14C were terminated by filtering the samples through 0.45 mm membrane filters, and the filtration vacuum was o100 mmHg. The filters were placed on the bottom of a glass scintillation vial which contained HCl to remove inorganic 14C. The filters with the organic 14C were kept frozen at –20 1C

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

and the membrane filters were digested with HCOOH for about 2.5 h. The samples were counted with a 2000 CA/LL Liquid Scintillation Analyzer, and primary productivity was calculated according to Parsons et al. (1984).

3. Results 3.1. Species composition and abundance One hundred and thirty-three species including 35 species of copepods and 98 other zooplankton species representing a total of 38 groups were identified (Table 1) in the wet season. Zooplankton larvae (including copepod nauplii, polychaete larvae, chaetognath larvae, etc.) represented 11% of the total zooplankton abundance. Copepods were the most dominant component of zooplankton in the study area, both in terms of species diversity and numerical abundance. Copepods accounted for at least 73% of the total zooplankton abundance in the water column, and copepodites and adults dominated the copepod populations. In the wet season, the average abundance of copepods was 1.3  104 individuals m
3. The maximum copepod abundance among the 31 sampling stations was 4.4  104 individuals m
3 at station 24 near Wanshan Islands, and 3.8, 3.4 and 3.0  104 individuals m
3 at stations 22, 21 and 19, respectively (Fig. 2). The highest zooplankton abundance, 5.3  104 individuals m
3, occurred west of Lantau Island, while the lowest was 0.08  104 individuals m
3 at station 1. Elevated abundances were found at stations 21, 22, 23 and 24 in the transect across the estuary in the outer region, from Gaolan Islands to Putai Islands, where abundance exceeded 3.5  104 individuals m
3. It implied that a front might have been encountered on this transect. In the dry season, the highest abundance of copepods was 1.0  104 individuals m
3 at station 13 and the next was 0.67  104and 0.55  104 individuals m
3 at stations 9 and 15, respectively. There was high abundance around station 13 (Fig. 3). The lowest abundance was 0.1  104 individuals m
3 collected at station 16. The cope-

1953

pod abundance was lower in the inner part of the estuary and increased towards the coastal stations, but a high abundance of 0.5  104 individuals m
3 was recorded at the inner stations 1, 2, 4 and 7. The average abundance was 3.9  103 individuals m
3 in the dry season. No obvious elevated abundance were recorded on the transect composed of stations 21, 22, 23 and 24, as was found in the wet season. In the wet season, the zooplankton were generally dominated by six copepod species, namely, Acartia spinicauda, Pavocalanus crassirostris, Oithona rigida, Paracalanus aculeatus, Euterpina acutifrons and Oithona setigera. Acartia spinicauda was the most dominant copepod in the estuary, constituting 23% of the total abundance of zooplankton. Three genera of copepods (Acartia, Paracalanus and Oithona) dominated the zooplankton community, accounting for 75% of the total copepod abundance. Acartiella sinensis was the dominant estuarine copepod in oligohaline regions with salinities o15. Estuarine marine species such as Acrocalanus gracilis and Paracalanus aculeatus were found in salinities ranging from 17 to 32. Other abundant estuarine marine species included Acartia spinicauda, Pseudodiaptomus poplesia, Pseudodiaptomus forbesi, Pavocalanus crassirostris, Oithona rigida, Euterpina acutifrons and Oithona setigera. Marine euryhaline copepods were found in salinities as low as 1. Other important zooplankton species in this estuarine system were Keratella cochlearis, Sagitta enflata, Lucifer hanseni, Oikopleura longicauda, Macrura larvae and meroplanktonic larvae of Polychaeta. The dominant species at the anchored stations C1–C3 were similar to the other stations. At different stations, the abundance of dominant species varied over time (Fig. 4). Copepods were especially abundant at C2 and C3, whereas C1 had the lowest copepod abundance. In dry season, only copepod assemblages were counted. A total of 30 species were collected at 21 stations. The community was dominated by Paracalanus serrulus, which composed up to 45% of the total copepod abundance. It is a species very similar to Paracalanus aculeatus, but it is considered a separate species based on some features of the body and it belongs to the autumn/winter

ARTICLE IN PRESS 1954

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

Table 1 List of ciliates, copepods, medusae and ctenophore species collected from the PRE during the summer of 1999 Copepoda

Decapoda

Siphonophora

Acartia spinicauda Acartiella sinensis Acrocalanus gibber Acrocalanus gracilis Bestiola sinicus Canthocalanus pauper Cyclopina tenuiremis Corycaeus affinis Corycaeus pacificus Calanopia elliptica Centropages sp. Clytemnestra scutellata Euterpina acutifrons Euchaeta concinna Labidocera euchaeta Microsetella rosea Nauplius larvae Oithona rigida Oithona setigera Oithona norvegica Oncaea venusta Pavocalanus crassirostris Paracalanus aculeatus Paracalanus serrulus Pseudodiaptomus poplesia Pseudodiaptomus forbesi Pseudodiaptomus sp. Pontellopsis tendicauda Pachysoma punctatum Subeucalanus subcrassus Scolecithricella longispinosa Temora discaudata Temora turbinate Tortanus gracilis Undinula vulgaris Medusa Medusetta spp. Heterotiara minor V. Pennaria tiarella (Ayres) Eirene hexanemalis (G.) Eutima levuka (A. et M.) Eucheilota spp. Phialucium spp. Liriope tetraphylla (Ch. et E.) Aglaura hemistoma P. et L. Muggiaea atlantica Cunningram Diphyes bojani (Eschscholtz) Diphyes chamissonis Huxley Diphyes dispar (Ch. et E.)

Acetes chinensis Hansen Acetes larvae Lucifer hanseni Nobili L. intermedius Hansen L. penicillifer Hansen Lucifer larvae Porcellana larvae Brachyura larvae Macrura larvae Macrura spp. Stomatopoda larvae Alima larvae Chaetognatha Pterosagitta draco (Kr.) Sagitta enflata Gr. S. pulchra Doncaster S. ferox Doncaster S. pacifica Tokioka S. bedoti Beraneck S. nagae Alvarinn S. neglecta Aida S. delicata Tokioka S. johorensis P.et T. Sagitta larvae Pseudoeuphausia larvae Biptinnaria larvae Asteroidea larvae Pentacula larvae Ophiuroidea larvae Tunicate Oikopleura longicauda (Vogt) O. dioica Fol O. rufescens Fol O. spp. Fritillaria spp. Doliolum denticulatum (Q. et G.) Thaliacea democratica Fishes larvae Fishes eggs Other eggs Ciliata Leprotintinnus nordguisti (Br.) Leprotintinnus spp. Tintinnopsis japonica Hada T. butchlii Daday T. karajacensis Brandt T. radix (Imhof) Pyrrophyta Noctiluca scintillans (k.et S.)

Diphyes spp. Hippopodiidae spp. Lensia subtilis (Chum) Chelophyes contorta (L.) Abylopsis spp. Actinula larvae Ctenophora Pleurobrachia globosa Moser sp. Beroe cucumis Fabricius Beroe sp. Rotatoria Brachionus spp. Keratella cochlearis (Gosse) Polychaeta Pelagobis longicirrata (Greeff) Pelagobis spp. Polychaeta larvae Bivalvia larvae Heteropoda Janthina janthina (Linnaeus) Atlanta rosea Souleyet Atlanta spp. Perotrochus spp. Pteropoda Limacina trochiformis (d0 O.) Limacina bulimoides (d0 O.) Limacina spp. Agadina syimpsoni (Adams) Creseis acicula (Rang) Peraclis reticulata (d’ O.) Gastropoda larvae Cephalopoda larvae Cladocera Penillia avirostris (Dana) Pseudevadne tergestina (Claus) Ostracoda Paravargula hirsata (Poulsen) Paravargula sp. Euconchoecia aculeata (Sc.) Ostracoda spp. Cirripedia larvae Mysis larvae Amphipoda Amphipoda larvae Vibilia spp. Lestrigonus spp. Amphithyrus spp.

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

1955

22.7

22.6

22.5 Hong Kong

22.4

22.3 Lantau Is 22.2

22.1

22

21.9

113.4

113.5

113.6

113.7

113.8

Fig. 2. Distribution of copepods as number of individuals m


3

113.9

114

114.1

114.2

114.3

114.4

114.5

in the summer wet season. Filled circles depict the sampling stations.

22.7

22.6

22.5 Hong Kong

22.4

22.3 Lantau Is 22.2

22.1

22

21.9

113.4

113.5

113.6

113.7
3

113.8

113.9

114

114.1

114.2

114.3

114.4

114.5

Fig. 3. Distribution of copepods (individuals m ) during the winter dry season. Filled circles depict the sampling stations.

ARTICLE IN PRESS 1956

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

salinity from 12 to 32 (Tan, unpubl. data); it was only found at stations 1 and 2 during the winter cruise. The distribution of copepod abundance at various sampling stations during the wet and dry seasons is illustrated in Fig. 5. 3.2. Zooplankton community

Fig. 4. Diel changes in the abundance of dominant zooplankton species at three anchored stations, C1, C2 and C3 during July 2000.

type. Pavocalanus crassirostris accounted for 22%, Paracalanus parvus for 11%, Acartia spinicauda and Oithona spp. for 5.4%. The genus Paracalanus was widely distributed in all sampling regions, while Corycaeus affinis was mainly distributed in the outer region of the estuary. B. sinicus is widely distributed in the coastal waters of Guangdong, including the inner bays and estuaries with water temperature ranging from 141C to 29.5 1C and

Zooplankton in the PRE can be separated to four groups according to their habitat as follows: Estuarine community: These species are adapted to a wide temperature range and low-salinity waters, and only a few species were founded in these waters. They are only distributed in a small region that was affected by land runoff. Representative species include, Acartiella sinensis, Acartia spinicauda, Oithona rigida, Penillia avirostris and Lucifer hanseni. Tropical neritic community: Species such as Temora discaudata, Temora turbinata, Calanopia minor, Paracalanus aculeatus, Cyclopina sp., Corycaeus affinis and Acrocalanus gibber were the most abundant and widely distributed, and occurred in the wet season with high water temperatures. Warm-temperate nearshore community: These species are adapted to lower temperatures and are not very abundant. Their distribution varies with the season, and they occur in winter, spring and occasionally in autumn. They are only found in the outer part of the PRE in summer. Representative species were Calanus sinica, Centropages tenuiremis and Labidocera euchaeta. Pelagic community: All these species occur in low frequency and abundance, in high salinities in spring and winter. A large number of species such as Subeucalanus subcrassus, Sagitta enflata, S. bedoti, Limacina spp., Diphyes chamissonis, Undinula vulgaris and Scolecithricella sp. were found in this area. Although the four communities co-occurred in these waters, species belonging to the tropical neritic community were more frequent, followed by estuarine low-salinity species such as Acartia spinicauda, Paracalanus aculeatus, Pavocalanus crassirostris, Oithona rigida and Euterpina acutifrons. The species richness was higher in the outer part of the estuary than in inner estuary (Table 2).

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

1957

Fig. 5. Copepod abundance at various sampling stations during the wet and dry seasons.

Table 2 Species richness, diversity index (H 0 ) and evenness (J) at different sampling stations in the PRE during winter and summer Station Species richness

H0

J

Station Species richness

Summer Winter Summer Winter Summer Winter 1 2 3 4 5 7 8 9 10 11 12 13 14 15 16 17

13 14 11 14 16 12 17 16 17 17 20 17 27 19 20 8

5 4 6 8 9 12 8 9 10 — — 6 8 9 11 10

1.42 2.05 1.65 1.95 2.07 1.66 2.02 2.02 1.63 1.53 2.1 2.04 1.98 0.64 1.07 1.68

1.34 1.30 2.11 2.03 2.64 1.46 1.60 1.09 2.01 — — 1.75 1.38 0.96 1.80 3.06

0.55 0.78 0.69 0.74 0.75 0.67 0.71 0.73 0.57 0.54 0.7 0.72 0.6 0.45 0.36 0.86

0.58 0.65 0.82 0.68 0.83 0.41 0.53 0.34 0.61 — — 0.68 0.46 0.30 0.52 0.92

A total of 21 species were recorded in the inner part, while 42 species were found in the outer regions. The species richness varied with season, with high species richness in the summer and low richness in the winter. B. sinicus was the dominant species in winter.

H0

J

Summer Winter Summer Winter Summer Winter 18 19 20 21 22 23 24 25 26 27 28 29 30 31 39

14 12 31 48 45 45 38 41 26 35 42 26 37 20 30

— 9 — — — 12 8 10 15 16 — — — — 14

1.77 0.88 2.61 2.29 2.1 2.28 2.13 2.29 1.7 2.17 3.16 2.21 2.39 1.23 1.77

— 1.31 — — — 1.36 1.66 1.65 2.35 2.28 — — — — 1.72

0.67 0.36 0.76 0.59 0.55 0.6 0.59 0.62 0.52 0.61 0.85 0.68 0.66 0.41 0.52

— 0.41 — — — 0.38 0.55 0.50 0.60 0.57 — — — — 0.45

3.3. Diversity index, eveness and richness Zooplankton taxa richness showed large fluctuations in the PRE; species richness ranged from 8 at station 17 to 48 at station 21 (the western mouth of the estuary) in summer (Table 2).

ARTICLE IN PRESS 1958

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

Copepod taxa richness also showed large fluctuations, ranging from 4 at station 1 to 17 at station 24. In general, the species richness at stations in the outer region of the estuary was higher than those in the inner regions. The diversity index (H 0 ) varied between 0.64 at station 15 to 3.16 at station 28, with an average of 1.94. The diversity index at stations 28, 29 and 30 (located in Dapeng Bay) was high, and more species were recorded at these stations than at other stations. The lowest evenness (J) (0.36) was found at stations 16 and 19, and the highest evenness (0.86) was recorded at station 17. The mean evenness of all sampling stations was 0.64. Both species richness and biodiversity increased towards the outer regions of the estuary, suggesting that most species in the estuary were of oceanic origin. The diversity index showed little difference among the stations in the outer region of estuary. Due to the low species richness, the evenness at the inner estuarine stations was somewhat higher than at the other stations. In the dry season, copepod species richness ranged from 4 at station 2 to 16 at station 27 (Table 2). The diversity index (H0 ) varied between 0.96 at station 15 and 3.06 at station 16, with an

average of 1.75. The diversity index at stations 16, 6 and 26 was high, and more species were recorded at these stations than at other stations. The lowest evenness (J) (0.30) was found at station 15, and the highest evenness (0.92) was estimated at station 16. The mean evenness of all sampling stations was 0.57. There was no significant difference for species richness and biodiversity between the inner and outer regions of the estuary, suggesting that the species were distributed with more evenness in the dry season than in the wet season. 3.4. Gut pigment content in copepods The copepod gut pigment level ranged from 4.2 ng Chl a ind
1 at station 27 to 0.24 ng Chl a ind
1 at station 13 in the wet season. The average gut content of the copepods in the estuary was 1.370.99 ng ind
1. Gut contents varied widely among the sampling stations. The gut pigments at all three anchored stations were lower than those measured at the other stations, especially at stations C1 and C3. Gut Chl a content displayed diurnal rhythms, both at stations C1 and C2, and there was higher gut fluorescence during the day than at night (Fig. 6).

Fig. 6. Diel variation in gut pigment content at three anchored stations C1, C2 and C3 during the wet season. Error bars represent 61 SD and n ¼ 3.

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

Gut pigment content was low during both day and night at station C3. In the dry season, the gut pigment content varied between 0.56 ng Chl a ind
1 at station 1 to 2.6 ng Chl a ind
1 at station 24. Replication was good since we obtained almost the same value of gut pigment content (0.63 ng Chl a ind
1) during the second sampling time at station 1 as compared to the first time. The gut pigments at stations 24, 25, 26 and 39 exceeded 2.0 ng Chl a ind
1. The gut pigment content between species showed a large variation (Fig. 7). Amongst the copepods, individual gut pigment concentrations ranged from 1.1 to 3.0 ng Chl a ind
1 in Subeucalanus subcrassus, from 0.63 to 1.6 ng Chl a ind
1 in Paracalanus serrulus and from 0.71 to 1.5 ng Chl a ind
1 in Acartia spinicauda. The average gut pigment content of single species picked from different stations ranged from 0.07 ng Chl a ind
1 in Pavocalanus crassirostris to 2.3 ng Chl a ind
1 in Calanus sinicus. The gut pigment content (G) in the copepods was significantly related to their body length (L); the regression equation was G ¼ 0:884 L þ 0:703, R2 ¼ 0:8037, n ¼ 10. According to the number of each species available in the sample, the gut pigment of Subeucalanus subcrassus was measured at eight stations, Paracalanus serrulus at 10 stations and gut pigment of the other species was measured less frequently for five stations. The gut pigment content of Subeucalanus subcrassus,

Paracalanus serrulus and Acartia spinicauda at different stations is shown in Fig. 7. 3.5. Ingestion rates and grazing impact Average hourly gut evacuation rates were 0.046 and 0.037 min
1 at station C1 and C3 measured over 4 h intervals. The evacuation rate constants varied between 0.079 and 0.017 min
1 at different time intervals over 24 h at station C2 in the wet season, with a mean value of 0.03970.008 min
1 (Fig. 8). The in situ daily ingestion rates were calculated from the gut pigment content and evacuation rate. There was no consistent pattern for the copepods’ ingestion rate at the three anchored stations (Fig. 9). Among the regular stations, the ingestion rates varied from 9.9 ng ind
1 h
1 at station 27 to 0.56 ng ind
1 h
1 at station 13, with a mean value of 3.072.33 ng ind
1 h
1. The amount of Chl a grazed by the four dominant species accounted for 85–94% of the total Chl a removal. By applying the mean gut evacuation constant of 0.039 min
1 to C1, C2, C3 and other stations, we calculated the copepod ingestion rates and their grazing impacts at these stations (Figs. 9 and 10). At the regular stations, the total hourly grazing represented o1.3% of the Chl a standing stock in the water column. The mean values of 33719.5% of phytoplankton stock were grazed by copepods on a daily basis at station C2. The highest daily grazing impact of 103% on the initial standing stock was recorded at station 22, and the lowest

2.5 0.12

2

1 0.5 0

C.

s sus ata da lus mis us mis tris sis u icu n s u ic r n sin bcras turbi inica . serr nuire . sin laefo ssiro sine B idu cra u A. s T. A.sp P C. te . . p S P cre P.

0.10

-1

1.5

Gut Evauation Rate (min )

Gut Chl a Content (ng ind-1)

3

1959

0.08 0.06 0.04 0.02 0.00 01:00

05:00

09:00

13:00

17:00

21:00

Time

Fig. 7. Average gut pigment content for different zooplankton species during the dry season. Error bars represent 61 SD and n ¼ 3.

Fig. 8. Diel variation of integrated gut evacuation rates at C2 in the wet season. Error bars represent 61 SD and n ¼ 3.

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

1960 2.0

40

C1

C1 1.5

30

1.0

20

.5

10

0.0 19:00

01:00

07:00

C2

8 6 4 2 0 12:00

18:00

0:00

06:00

0

13:00

12:00

% Removed by Copepod Grazing

Ingestion Rate(ng ind-1 h-1)

13:00

13:00

19:00

01:00

07:00

13:00

100

C2 80 60 40 20 0

80

12:00

18:00

0:00

06:00

12:00

C3

1.2

C3 1.0

60

.8

40 .6 .4

20

.2

0

0.0 14:00 17:00 20:00 23:00 08:00 11:00 14:00

14:00 17:00 20:00 23:00 08:00 11:00 14:00

Time

Time Fig. 9. Diel variation of ingestion rates at three anchored stations C1, C2 and C3 in the wet season. Error bars represent 61 SD and n ¼ 3.

(0.64% and 0.97%) at stations 1 and 2. An average daily grazing impact for total zooplankton and copepods were calculated to be 26729.5% and 20721.5% at the regular stations, respectively. The average copepod grazing impact on primary productivity was 27749% and percent productivity grazed was lower in winter than summer (Fig. 11A and B). The mean daily grazing of

Fig. 10. Daily grazing impact (as %) on phytoplankton standing stock based on Chl a, at three anchored stations C1, C2 and C3. Error bars represent 61 SD and n ¼ 3.

copepods on phytoplankton standing stocks was 13710.1% at C1, and 27715.5% at C3 (Fig. 10). The average evacuation rate of the mixed species at the three stations in the dry season was lower than the wet season, with a mean value of 0.032 min
1. Similarly, the value was applied to calculate the ingestion rates in other stations where no in situ evacuation experiment was conducted.

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

1961

Summer 22.7

22.6

22.5 Hong Kong

22.4

22.3 Lantau Is 22.2

22.1

22

21.9

21.8 113.4

113.5

113.6

113.7

113.8

113.9

114

114.1

114.2

114.3

114.4

114.5

(A) Winter 22.7

22.6

22.5

22.4

Hong Kong

22.3 Lantau Is 22.2

22.1

22

21.9

(B)

113.4

113.5

113.6

113.7

113.8

113.9

114

114.1

114.2

114.3

114.4

114.5

Fig. 11. Spatial distribution of copepod daily grazing impact as % Chl removal in different seasons, (A) summer and (B) winter. Chl a and primary productivity (PP).

The highest ingestion rate was 5.7 min
1 at station 39 and the lowest was 0.19 min
1 calculated for the second sampling time at station 1. The grazing impact was calculated by multiplying the domi-

nant copepod herbivore abundance, ingestion rates and dominance of the individual at the stations. The average daily grazing impact of copepods on Chl a standing stock was lower

ARTICLE IN PRESS 1962

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

during the dry season than during the wet season, with a value of 4.573.2% at 21 sampling stations (Fig. 12A). This is equivalent to 4.874.7% of the total daily primary production (Fig. 12B). Difference in the grazing impact on the daily primary productivity and phytoplankton standing stock of copepod between seasons is shown in Fig. 12. The highest grazing impact along the transect was recorded within the frontal zone where zooplankton removed between 11.5% and 103% of the Chl a standing stock in the summer (Fig. 11A) and between 1.4 and 6.4% each day in the winter (Fig. 11B).

The results indicate that the copepods had a strong effect on the phytoplankton standing stocks in the estuary in the wet season and a minor impact on phytoplankton standing stocks in the dry season. The difference in results between the two seasons will be discussed later. 3.6. Individual ingestion rates and grazing impact We measured the individual ingestion rates and grazing impact in the dry season. The ingestion rates of individuals ranged from 2.2 to 5.7 min
1 for Subeucalanus subcrassus, from 1.4 to 2.8 min
1 for Acartia spinicauda and from 1.1 to 3.1 min
1 in

Fig. 12. Copepod daily grazing impact as % Chl and primary productivity removed in the wet and dry seasons.

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

Paracalanus serrulus. We only illustrated the daily grazing impact for three species due to species availability in the sample from different stations. The value of the grazing impact on Chl a standing stock was usually close to that of primary productivity for any of the three species. Paracalanus serrulus had a higher grazing impact, both on Chl a standing stock and primary productivity than the other two species, with a mean value of the grazing impact of 3.472.9% on the Chl a stock and 3.372.9% of primary productivity,

1963

respectively (Fig. 13). The grazing impact of Para serrulus varied from 10% at station 27 to 0.25% at station 2. The highest grazing impact of Acartia spinicauda was 0.7% at station 4 and the lowest was about 0.15% at station 5 (Fig. 13). Subeucalanus subcrassus contributed 0.27% with the highest grazing impact at station 15 and 0.02% as the lowest impact at station 9. Acartia spinicauda grazed 0.2270.27% of the Chl a standing stock and 0.3370.44% of the primary productivity each day. Subeucalanus subcrassus only grazed 0.127 0.12% Chl a standing stock and 0.1370.20% primary productivity.

4. Discussion 4.1. Species composition and abundance

Fig. 13. Grazing impact (as %) of three copepod species on phytoplankton at various stations.

In the PRE, the zooplankton abundance was higher and patchier than those reported in other areas, especially at station C2 where swarms occurred. Swarm behavior of mixed copepod populations has been observed in shallow water in tropical and subtropical regions (Kimoto et al., 1988). Oithona rigida co-occurred with Acartia spinicauda and in large numbers (106 individuals m
3) in this study. Cyclopoid copepods of the genus Oithona often swarm with Acartia (Omori and Hamner, 1982). In addition, boundaries or fronts in estuaries may affect the distribution of copepods. Aggregations of copepods and other zooplankton tend to occur at boundaries or fronts in the vertical or horizontal planes (Petipa, 1985). Our average abundance of copepods was higher in summer than that observed during January, suggesting that there may be a seasonal descent of some species. Furthermore, copepod abundance was more affected by environmental factors in the stratified layer than in other parts of the water column. During the rainy season, freshwater from Pearl River flows over the oceanic waters from the South China Sea, and therefore a strong vertically stratified water column was observed in July. Salinity of the surface water dropped to 3.0, while salinity in the bottom layer ranged from 1.1 to 28.5 in the inner region of estuary, and therefore salinity was one of the most

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

1964

important physical factors affecting zooplankton abundance and species richness in this estuary (Fig. 14A). Thus, copepod abundance varied with the different water masses. Tidal currents can affect copepod distribution and feeding behavior (Petersen et al., 1998). Calanus sinicus and Labedocera euchaeta were most abundant in January 1992 (Fu et al. 1995), while Paracalanus serrulus and Pavocalanus crassirostris were the dominant species in our study in January. In the PRE, the diel changes in abundance of the dominant species may have resulted from the salinity or turbulence caused by the tidal actions. For example, the animals may move to the bottom during ebb tide, but then move upwards to the water column during flood tide (Kimmerer and Mckinnon, 1987; Hough and Naylor, 1992). Salinity and light attenuation correspond to the turbulence in the PRE, where high flow speeds corresponded with high salinities and light at60

40

Species Richness

20 y = 16.55+0.722x 2 r = 0.452 0 0

10

20 Salinity

30

40

60

40

20 y = 14.78 + 1.598x 2 r = 0.391 0 0

2

4

6

8

10 12 14 16 18

1% Light Attenuation Depth(m) Fig. 14. Relationship between zooplankton species richness and salinity or light attenuation during the wet season at regular stations.

tenuation. Salinity and flow speed had similar diel fluctuation patterns at station C1. 4.2. Gut pigment content The estimates of gut contents at our sampling stations were within the range of those reported for other estuaries (Dagg, 1995; Froneman, 2001), and were low with respect to the Chl a concentration in this area. Gut pigment content was low at the anchored stations compared to that of the other stations. The low gut capacities may have been caused by experimental losses during the sampling transfer. Other reasons could be the food concentration, the total zooplankton abundance or the ambient environment. Gut Chl a content displayed diurnal rhythms both at stations C1 and C2, and there was a higher gut fluorescence during the day than at night. Gut pigment contents were low during both day and night at station C3. It may be due to the lowest water depth and lowest current speed at station 3. Gut pigment was not associated with Chl a or phytoplankton abundance, except at station C1. This implied that other factors such as currents and diel rhythms affect the feeding of the copepods. The highest variability in both plankton composition and Chl a concentration was found at station C3, probably due to displacements of the front and currents that can clearly influence the feeding behavior. Gut pigment content can vary widely depending on feeding history, food concentration, light, diel feeding behavior and turbulence (Wang and Conover 1986; Kiørboe and Tiselius, 1987; Head, 1992; Head and Harris, 1996). High turbulence can eliminate the feeding currents, resulting in lower clearance and lower ingestion rates (Kiørboe and Saiz, 1995). Fluctuations in gut contents may be attributed to the influence of a combination of several factors such as endogenous rhythms (Duval and Geen, 1976) and intermittent periods of grazing activity (Boyd and Smith, 1980; Mackas and Burns, 1986; Sautour et al., 1996). 4.3. Ingestion rates and grazing impact For the evacuation experiment at station C2, feeding began simultaneously with nocturnal

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

ascent at approximately 16:00, when the relative change in ambient light intensity was the greatest. Similarly, feeding was more active during the night than during the day at stations C1 and C3. Likewise, several studies have noted the nocturnal feeding in copepods (Head et al., 1985, Dam and Peterson, 1993), with the ingestion rate increasing as light intensity decreases. Mean ingestion rates during night time were significantly higher than during the day at anchored stations. Dam and Peterson (1993) indicated that Temora longicornis in Long Island Sound usually fed throughout the day, with comparable feeding rates during day and night. Copepods exerted a moderate predation pressure on the phytoplankton at the mouth of the PRE. The grazing activity of copepods varied with the time of the day and the ambient food concentration, and was within the range of 0.05–11% (Wong et al., 1998), or 2.9–13% (Wang et al., 1998), or 5–40% (Bautista and Harris, 1992). The daily grazing impacts of copepods on the phytoplankton fluctuated from 0.64% to 103% at our sampling stations, and represented an average of 26729% of the phytoplankton standing stock in the summer. Mean Chl a values of 13710%, 33719% and 27715% were grazed daily at stations C1, C2 and C3, respectively. Grazing pressure exerted by copepods on phytoplankton was consistently low in winter, only 0.5% to 21% of primary production was grazed by the copepod assemblage. In contrast, grazing by mesozooplankton can contribute 35–68% of the phytoplankton stock and 1075% of the daily primary productivity in the Gironde estuary (Sautour et al., 1996, 2000). The impact of grazing on phytoplankton by mesozooplankton, including copepods, can be variable. The impact of copepod grazing can match or even exceed the daily primary productivity (Dagg and Turner, 1982; Hansen et al., 2000; Kiørboe and Nielsen, 1994). The daily grazing impact on the phytoplankton was generally high at our sampling stations during the summer wet season cruise and grazing pressure exerted by copepods on phytoplankton was consistently low during the dry season, because a key factor in determining the level of grazing is the copepod abundance at the time of sampling

1965

(Gowen et al., 1999), although the ingestion rates (3.072.3 ng ind
1 h
1 in summer and 2.37 2.1 ng ind
1 h
1 in winter) were comparable to previous studies. Actually, we had observed a high density of copepods in the samples used to determine Chl a and phytoplankton at the stations with a higher grazing impact such as station C2 and adjacent waters. Another possible source for overestimating or underestimating the grazing impact of copepod community is that grazing by herbivores was assumed to be approximately 65% of the total zooplankton; this value may vary between stations and seasons. Although copepods accounted for at least 73% of the total zooplankton abundance in both seasons in our study, we used the mean evacuation rate of copepods to estimate that of other mesozooplankton groups such as polychaetes and amphipods and this could have introduced errors in the grazing impacts. The average clearance rate constant at station C2 in summer and three stations in winter were used to calculate the ingestion rate of the other stations, which could also be a reason to underestimate the grazing impact. Copepod consumption of phytoplankton biomass varied widely in these cruises. Feeding, however, was not strictly a function of phytoplankton availability because copepods fed better at station C2 where Chl a concentrations were somewhat lower (1.7 mg m
3) than at station C3 where Chl a was 2.1 mg m
3 at the same time (16:30), although phytoplankton species at these stations were dominanted by Skeletonema costatum, Nitzschia pungens, N. delicatissima and Asterionella japonica. These data confirm that other biotic or abiotic factors affected the feeding rates of zooplankton. A correlation analysis indicated that a high value of Chl a usually coincided with a low ingestion rate in our study. However, phytoplankton are not the only available food for zooplankton (Penry and Frost, 1990). Few copepods are purely herbivorous, and heterotrophic flagellates, ciliates and nauplii can also be food sources for zooplankton. Hence, we used 67% to estimate the number of herbivorous zooplankton in our study. The impact of grazing on phytoplankton by mesozooplankton, including copepods, has been reported for other marine environments and has been shown to be highly

ARTICLE IN PRESS 1966

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

variable. Similarly, turbulence and light intensity affected the ingestion rates and grazing impacts. Turbulent water motion enhances the encounter rates between planktonic organisms and their food (Rothschild and Osborn, 1988), altering the perception of the food environment for copepods and other planktonic animals (Hwang et al 1994; Strickler and Costello, 1996). As a consequence, their feeding behavior is affected, and the grazing rates are significantly increased. On the other hand, if a C:Chl conversion ratio of 50 or 100 is used, the feeding pressure would have increased (3–5 fold) to exceedingly high levels. Where does primary production that is not grazed by copepods go, especially in winter? Three likely sinks for ungrazed phytoplankton are: (1) other mesozooplankton; (2) grazing by microzooplankton; and (3) sedimentation and subsequent utilization by the benthic fauna or decomposition by bacteria as stated above. Microzooplankton have been shown to graze a substantial amount of phytoplankton, especially in nearshore environments (e.g. Gifford, 1988; Dagg, 1995). In the Canadian Arctic, microzooplankton grazed from 37% to 114% of the primary production (Paranjape, 1987), and along a transect in the Bellingshausen Sea, microzooplankton were estimated to graze between 21% and 271% of phytoplankton production (Burkill et al., 1995). It is well known that grazing impact varies seasonally and can also reflect the high degree of variability in the spatial distribution of consumers and primary production levels in the region (Landry et al.,1994; Perissinotto, 1992; Ward et al., 1995). It was shown that average copepod abundance was 1.4  104 ind m
3 in summer, and it decreased to 3.9  103 ind m
3 in winter. Water column Chl a was about 5 mg m
3 both in winter and summer. Copepods can graze an average of 26730% of the phytoplankton standing stock in the study waters. At some stations, more than 76% of the chlorophyll standing stock or up to 104% of the daily phytoplankton production was removed by copepods in summer. It suggests that copepods play an important role in controlling the phytoplankton blooms in the wet season, which could help to decrease the occurrence of red tides blooms in this region.

As a consequence of the high copepod abundance, much of the phytoplankton stock may be transferred to higher tropic levels by copepod grazing during the wet season in the PRE. During January 2001, the estimated grazing impact was not sufficient to control phytoplankton production at any one station. While zooplankton grazing could not control phytoplankton growth, probably physical factors were responsible for the decline of any small blooms.

Acknowledgments This study was financially supported by the Pearl River Estuary Pollution Project (PREPP) from the Hong Kong Jockey Club, the fund of National Key Basic Research Project (2001CB409707) and fund 40106015 from the National Science Foundation of China. We thank Dr. Wen-xiong Wang and Professor Paul Harrison who made helpful comments on an earlier version of the manuscript.

References Atkinson, A., Ward, P., Murphy, E.J., 1996. Diel periodicity of subantarctic copepods: relationships between vertical migration, gut fullness and gut evacuation rate. Journal of Plankton Research 18, 1387–1405. Bathmann, U.V., Noji, T.T., Bodungen, B., 1990. Copepod grazing potential in late winter in the Norwegian Sea: a factor in the control of spring phytoplankton growth?. Marine Ecology Progress Series 60, 225–233. Bautista, B., Harris, R.P., 1992. Copepod gut contents, ingestion rates and grazing impact on phytoplankton in relation to size structure of zooplankton and phytoplankton during a spring bloom. Marine Ecology Progress Series 82, 41–50. Bays, J.S., Crisman, T.L., 1983. Zooplankton and trophic state relationships in Florida lakes. Canadian Journal of Fisheries and Aquatic Science 40, 1813–1819. Beaver, J.R., Crisman,, T.L., 1982. The trophic response of ciliated protozoans in freshwater lakes. Limnology and Oceanography 27, 246–253. Boyd, C.M., Smith, S.L., 1980. Plankton, upwelling, and coastally trapped waves off Peru. Deep-Sea Research 30A, 723–742. Breitburg, D.L., Sanders, J.G., Gilmour, C.C., Hatfield, C.A., Osman, R.W., Riedel, G.F., Seitzinger, S.P., Sellner, K.G., 1999. Variability in responses to nutrients and trace elements, and transmission of stressor effects through an

ARTICLE IN PRESS Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968 estuarine food web. Limnology and Oceanography 44, 837–863. Burkill, P.H., Edwards, E.S., Sleigh, M.A., 1995. Microzooplankton and their role in controlling phytoplankton growth in the marginal ice zone of the Bellingshausen Sea. Deep-Sea Research II 42, 1277–1290. Dagg, M.J., 1995. Ingestion of phytoplankton by the microand mesozooplankton communities in a productivity subtropical estuary. Journal of Plankton Research 17, 845–857. Dagg, M.J., Turner, J.T., 1982. The impact of copepod grazing on the phytoplankton of Georges Bank and the New York Bight (USA). Canadian Journal of Fisheries and Aquatic Sciences 39, 979–990. Dam, H.G., Peterson, W.T., 1988. The effect of temperature on gut clearance rate constant of planktonic copepod. Journal of Experimental Marine Biology and Ecology 123, 1–14. Dam, H.G., Peterson, W.T., 1993. Seasonal contrasts in the diel vertical distribution, feeding behavior, and grazing impact of copepods Temora longicornis in Long Island Sound. Journal of Marine Research 51, 561–594. Duval, W.S., Geen, G.H., 1976. Diel feeding and respiration rhythms in zooplankton. Limnology and Oceanography 21, 823–829. Froneman, P.W., 2001. Seasonal changes in zooplankton biomass and grazing in a temperate estuary, South Africa. Estuarine, Coastal and Shelf Science 52, 543–553. Fu, Y.Y., Yin, J.Q., Chen, Q.C., Huang Liangmin et al., 1995. Distribution and seasonal variation of marine zooplankton in the Pearl River estuary, Environmental Research in Pearl River estuary and Coastal Areas, Guangzhou: Guangdong Higher Education Press, 25–33. Gowen, R.J., McCullough, G., Kleppel, G.S., Houchin, L., Elliott, P., 1999. Are copepods important grazers of the spring phytoplankton bloom in the western Irish Sea?. Journal of Plankton Research 21, 465–483. Gifford, D.J., 1988. Impact of grazing by microzooplankton in the Northwest arm of Halifax Habour, Nova Scotia. Marine Ecology Progress Series 47, 249–258. Hansen, B.W., Hygum, B.H., Brozek, M., Jensen, F., Rey, C., 2000. Food web interaction in a Calanus finmarchicus dominated pelagic ecosystem—a mesocosm study. Journal of Plankton Research 22, 569–588. Harris, R.P., Malej, A., 1986. Diel patterns of ammonium excretion and grazing rhythms in Calanus helgolandicus in surface stratified waters. Marine Ecology Progress Series 31, 75–85. Head, E.J.H., 1992. Gut pigment accumulation and destruction by arctic copepods in vitro and in situ. Marine Biology 112, 583–592. Head, E.J.H., Harris, L.R., 1996. Chlorophyll destruction by Calanus spp. grazing on phytoplankton: kinetics, effects of ingestion rate and feeding history, and a mechanistic interpretation. Marine Ecology Progress Series 135, 223–235. Head, E.J.H., Harris, L.R., Abou Debs, C.A., 1985. Effect of daylength and food concentration on in situ diurnal feeding

1967

rhythms in Arctic copepods. Marine Ecology Progress Series 24, 281–288. Holmes, P.R., Lam, C.W.Y., 1985. Red tides in Hong Kong waters—response to a growing problem. Asian Marine Biology 2, 1. Hough, A.R., Naylor, E., 1992. Endogenous rhythms of circadial swimming activity in the estuarine copepod Eurytemora affinis. Journal of Experimental Marine Biology and Ecology 161, 27–32. Hwang, J.S., Costello, J.H., Strickler, J.R., 1994. Copepod grazing in turbulent flow: elevated foraging behavior and habituation of escape response. Journal of Plankton Research 16, 421–431. Kilham, S.S., Kilham, P., 1984. The importance of resource supply rates in determining phytoplankton community structure. In: Meyers, D.G., Strickler, J.R., (Eds.), Trophic Interactions within Aquatic Ecosystems, AAAS Selected Symposium Series, vol. 85, pp. 7–28. Kimmerer, W.J., Mckinnon, A.D., 1987. Zooplankton in marine bay. II. Vertical migration to maintain horizontal distributions. Marine Ecology Progress Series 41, 53–60. Kimoto, K., Nakashima, J., Morioka, Y., 1988. Direct observations of copepod swarm in small inlet of Kyushu, Japan. Bulletin of the Seikai Regional Fisheries Research Laboratory 66, 41–55. Kiørboe, T., Nielsen, T.G., 1994. Regulation of zooplankton biomass and production in a temperate, coastal ecosystem, 1. Copepods. Limnology and Oceanography 39, 493–507. Kiørboe, T., Saiz, E., 1995. Planktivorous feeding in calm and turbulent environments, with emphasis on copepods. Marine Ecology Progress Series 122, 135–145. Kiørboe, T., Tiselius, P.T., 1987. Gut clearance and pigment destruction in a herbivorous copepod Acartia tonsa and the determination of in situ grazing rates. Journal of Plankton Research 9, 525–534. Landry, M.R., Lorenzen, C.J., Peterson, W.K., 1994. Mesozooplankton grazing in the Southern California Bight. II. Grazing impact. Marine Ecology Progress Series 115, 73–85. Ma, K.P., 1994. Measure Methods of the biodiversity: I. Measure of a-diversity(1). Biodiversity Science 2 (3), 162–168 (In Chinese). Mackas, D.L., Bohrer, R., 1976. Fluorescence analysis of zooplankton gut contents and an investigation of diel feed patterns. Journal of Experimental Marine Biology and Ecology 25, 77–85. Mackas, D.L., Burns, K.E., 1986. Poststarvation feeding and swimming activity in Calanus pacificus and Metridia pacifica. Limnology and Oceanography 31, 383–392. Mauchline, J., 1998. The biology of calanoid copepods. Advances in Marine Biology 33, London: Oxford Press, pp. 188–192. Morales, C.E., Harris, R.P., 1990. A review of the gut fluorescence method for estimating ingestion rates of planktonic herbivores. ICES, Council Meeting, 1990, 12pp. Morales, C.E., Harris, R.P., Tranter, P.R.G., 1993. Copepod grazing in the oceanic northwest Atlantic during a 6 week

ARTICLE IN PRESS 1968

Y. Tan et al. / Continental Shelf Research 24 (2004) 1949–1968

drifting station: the contribution of size classes and vertical migrants. Journal of Plankton Research 15, 185–211. Nejstgaard, J.C., Bamstedt, U., Bageoien, E., Solberg, P.T., 1995. Algal constraints on copepod grazing. Growth state, toxicity, cell size, and season as regulating factors. ICES Journal of Marine Science 52, 347–357. Omori, M., Hamner, W.M., 1982. Patchy distribution of zooplankton: behavior, population assessment and sampling problem. Marine Biology 72, 193–200. Pace, M.L., 1986. An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnology and Oceanography 31, 45–55. Park, G.S., Marshall, H.G., 2000. Estuarine relationships between zooplankton community structure and trophic gradients. Journal of Plankton Research 22, 121–136. Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford 187pp. Paranjape, M.A., 1987. Grazing by microzooplankton in the eastern Canadian Arctic in summer 1983. Marine Ecology Progress Series 40, 239–246. Penry, D.L., Frost, B.W., 1990. Re-evaluation of the gutfullness (gut fluorescence) method for inferring ingestion rates of suspension-feeding copepods. Limnology and Oceanography 35, 1207–1214. Perissinotto, R., 1992. Mesozooplankton size-selectivity and grazing impact on the phytoplankton community of the Prince Edward Archipelago (Southern Ocean). Marine Ecology Progress Series 79, 243–258. Peter, J.S.F., 2001. Phytoplankton blooms in a fluctuating environment: the roles of plankton response time scales and grazing. Journal of Plankton Research 23, 1433–1441. Petersen, J.E., Sanford, L.P., Kemp, W.M., 1998. Coastal plankton responses to turbulent mixing in experimental ecosystems. Marine Ecology Progress Series 171, 23–41. Petipa, T.S., 1985. Production and concentration of plankton at boundary water masses: perspectives of investigation. In: Gibbs, P.E. (Ed.), Proceedings of Nineteenth European Marine Biology Symposium. Cambridge University Press, Cambridge, MA, pp. 61–71.

Pielou, E.C., 1966. The measurement of diversity in different types of biological collections. Journal of Theoretical Biology 13, 131–144. Rothschild, B.J., Osborn, T.R., 1988. Small-scale turbulence on feeding and gross growth efficiency of three Acartia species (Copepoda: Calanoid). Journal of Plankton Research 14, 1085–1097. Sautour, B., Artigas, F., Herbland, A., Laborde, P., 1996. Zooplankton grazing impact in the plume of dilution of the Gironde estuary (France) prior to the spring bloom. Journal of Plankton Research 18, 835–853. Sautour, B., Artigas, L.F., Delmas, D., Herbland, A., Laborde, P., 2000. Grazing impact of micro- and mesozooplankton during a spring situation in coastal waters off the Gironde estuary. Journal of Plankton Research 22, 531–552. Strickler, J.R., Costello, J.H., 1996. Calanoid copepod behavior in turbulent flows. Marine Ecology Progress Series 139, 301–312. Uye, S., 1986. Impact of copepod grazing on the red-tide flagellate Chattonella antiqua. Marine Biology 92, 35–43. Wang, R., Conover, R.J., 1986. Dynamics of gut pigments in the copepod Temora longicornis and the determination of in situ grazing rates. Limnology and Oceanography 31, 867–877. Wang, R., Li, C., Wang, K., Zhang, W., 1998. Feeding activities of zooplankton in the Bohai Sea. Fisheries Oceanography 7, 265–271. Ward, P., Atkinson, A., Murray, A.W.A., Wood, A.G., Williams, B., Poulet, S.A., 1995. The summer zooplankton community South Georgia: biomass, vertical migration and grazing. Polar Biology 15, 195–208. Wong, C.K., Hwang, J.S., Chen, Q.C., 1998. Taxonomic composition and grazing impact of calanoid copepods in coastal waters near nuclear power plants in Northern Taiwan. Zoological Studies 37, 330–339. Zhang, F., Dickman, M.D., 1999. Mid-ocean exchange of container vessel ballast water. I. Seasonal factor affecting the transport of harmful diatoms and dinoflagellates. Marine Ecology Progress Series 176, 243–251.