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Seasonal dynamics of zooplankton and grazing impact of microzooplankton on phytoplankton in Sanmen Bay, China
ACTA ECOLOGICA SINICA Volume 26, Issue 12, November 2006 Online English edition of the Chinese language journal Cite this article as: Acta Ecologica Sinica, 2006, 26(12), 3931−3941.
RESEARCH PAPER
Seasonal dynamics of zooplankton and grazing impact of microzooplankton on phytoplankton in Sanmen Bay, China Liu Zhensheng1,2,3, Wang Chunsheng2,3, Zhang Zhinan1, Liu Chenggang2,3, Yang Guanming2 1 College of Marine Life Science, Ocean University of China, Qingdao 266003, China 2 Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China 3 Key Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou 310012, China
Abstract: The species composition, biomass, abundance and species diversity of zooplankton were determined for samples collected from 12 stations in Sanmen Bay, China, in four cruises from August 2002 to May 2003. Growth of phytoplankton and grazing rates of microzooplankton were measured using the dilution technique. The spatial and temporal variation of zooplankton and its relationship with environmental factors were also analyzed. The results showed that a total of 89 species of zooplankton belonging to 67 genera and 16 groups of pelagic larvae were found in Sanmen Bay. The coastal low-saline species was the dominant ecotype in the study area, and the dominant species were Calanus sinicus, Labidocera euchaeta, Tortanus derjugini, Acartia pacifica, Pseudeuphausia sinica and Sagitta bedoti. Maximum biomass was recorded in August, followed by November and May, and the lowest biomass was recorded in February. Similarly, the highest abundance of zooplankton was observed in August, followed by May, November, and February. Grazing pressure of microzooplankton on phytoplankton in Sanmen Bay existed throughout the year, although the grazing rate of microzooplankton on phytoplankton varied with the season. Estimates for growth rate of phytoplankton －1
ranged from 0.25 d
to 0.89 d 1, whereas grazing rate of microzooplankton ranged between 0.18 d
－1
－
－1
and 0.68 d
in different sea-
sons. The growth rate of phytoplankton exceeded the grazing rate of microzooplankton in all the seasons. Grazing pressure of mi－1
crozooplankton on phytoplankton ranged from 16.1% d production of phytoplankton ranged from 58.3% d
－1
－1
to 49.1% d －1
to 83.6% d
, and the grazing pressure of microzooplankton on primary
in different seasons.
Key Words: zooplankton; biomass; abundance; microzooplankton grazing; Sanmen Bay
1
Introduction
Sanmen Bay is a half-closed bay located on the coast of middle Zhejiang Province, China. The drainage basin of this bay is about 3160 km2, and there are more than 30 streams flowing into the Sanmen Bay. The area of this bay is about 775 km2, and the average water depth is 5–10 m. As one of the most important aquiculture bases of the Zhejiang Province, the Sanmen Bay possesses conducive environmental conditions for the growth of marine plankton. Zooplankton plays a key role in the marine food web. Both the primary production and the aquatic product (fishery) are restricted by variations in the community structure of zooplankton. Furthermore, grazing of
microzooplankton plays an important role in material cycle and energy flow in the marine ecosystem. Since the 1980’s, there have been few studies on zooplankton in the Sanmen Bay. To the best of our knowledge, only few reports have been published thus far on the seasonal variation and grazing － rate of zooplankton in the Sanmen Bay[1 3 ]. This study investigates the community structure, seasonal variations in biomass, abundance, dominant species, diversity index, and grazing rate of zooplankton and discusses the relationship between zooplankton and environmental conditions. The results obtained in this study are useful and significant to evaluate the aquiculture ecosystem in Sanmen Bay, China.
Received date: 2005-09-12; Accepted date 2006-03-10 *Corresponding author. E-mail: [email protected] Copyright © 2006, Ecological Society of China. Published by Elsevier BV. All rights reserved.
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
2
Materials and methods
Four cruises were conducted from August 2002 to May 2003 to investigate the zooplankton population in Sanmen Bay (Fig. 1). Zooplankton samples from 12 stations were collected with vertical hauls of plankton nets (0.505 mm mesh, and 0.50 m mouth diameter) from the bottom to the surface, and then the samples were fixed with 5% formalin in plastic bottles (600 cm3). The biomass of zooplankton was measured and the species were identified at the laboratory following the National Standard of People’s Republic of China [GB 12763.6 -91][4].
Grazing pressure of microzooplankton on phytoplankton was calculated by[6]: Pi = (1-eg) × 100% Grazing pressure of microzooplankton on primary production was calculated by[6]: Pp = [ek-e(k-g)]/(ek-1) × 100% Diversity index and evenness index were calculated using the formulae of Shannon-Weaver and Pielou: S
H ′ = −∑( Pi )log 2 ( Pi ) i =1
J = H ′ / log 2 S Where Pi is the ratio between the species of one kind of plankton and the total species of plankton, and S is the number of species. The Sanmen Bay was divided into three zones: upper bay (S14, S15, S16), middle bay (S7, S9, S12, S18), and lower bay (S1, S2, S3, S5, S10).
3
Fig. 1 Investigation stations in Sanmen Bay, China
Grazing rates of microzooplankton were measured using the dilution technique developed by Landry and Hassett[5], in which samples were collected at the beginning and the end of the experiment for concentration of chlorophyll a. Replicate dilution treatments of 0.25, 0.5, 0.75, and 1.0× natural seawater were prepared in polycarbonate bottles. Measured amounts of water, which was filtered using the GF/F glassfiber membrane, was added to the experimental bottles; subsequently, the bottles were gently filled and mixed with unfiltered seawater. The water samples used for the dilution experiments were collected from middle of Sanmen Bay. The grazing rates of the microzooplankton were calculated by: Pt = Po e(k-dg)t Where Pt and Po are the final and the initial existing stock of phytoplankton, respectively, k is the growth rate of the phytoplankton, g the grazing rate of the microzooplankton, and d the dilution[6].
Results and discussion
3.1 Composition and community structure of zooplankton species 3.1.1 Species composition A total of 89 species of zooplankton, belonging to 67 genera and 16 groups of pelagic larvae, were found in Sanmen Bay. Copepods were found to be the dominant group among the zooplankton, with 36 species of this group being identified. In addition, species of pelagic larvae (16), Hydromedusae (15), Siphonophora (6), Decapoda (6), Tunicata (5), Pelagic mollusca (5), Chaetognatha (4), Ctenophora (2), Polychaeta (2), Cladocera (2), Mysidacea (2), Amphipoda (2), Cumacea (1), and Euphausiacea (1) were also identified (Table 1, Table 2). All groups of zooplankton in Sanmen Bay showed a marked seasonal variation. Most species of zooplankton were found in August when high water temperature and the invasion of offshore seawater were observed, resulting in an increase of warm water species and offshore species. Seventy-three species of zooplankton and 14 groups of pelagic larvae were found, including 48 species of copepods and medusae. A greater number of species of zooplankton were found in May (33 species of zooplankton and 12 groups of pelagic larvae) than in November (31 species of zooplankton and 5 groups of pelagic larvae), which was mainly because of medusae and pelagic larva. With a decrease in water temperature in February,
Table 1 Zooplankton composition and seasonal variation in Sanmen Bay, China (Aug. 2002 to May 2003) Time
Group Copepods
Medusae
Pelagic larva
Other groups
3
2
15
3
12
7
45
21
4
14
25
87
4
4
5
8
36
Feb. 2003
10
May 2003
16
7
Aug. 2002
23
Nov. 2002
15
Chaetognatha
Total
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Table 2 Species of zooplankton in Sanmen Bay, China (Aug. 2002 to May 2003) Species
Feb.
May
Aug.
Nov.
Hydromedusae 1. Sarsia nipponica Uchida
+
2. Ectopleura sp.
+
3. Euphysa aurata Forbes
+
4. Turritopsis nutricula McCrady
+
5. Clytia hemisphaericum Linnaeus
+
6. Obelia spp.
+
7. Phialucium sp.
+
8. Octophialucium indicum Kramp
+
9. Eirene ceylonensis Browne
+
10. Eutima (Otorchis) gegenbauri Haechel
+
11. Aequorea conica Browne
+
12. Aeginum sp.
+
13. Liriope tetraphylla Chamisso et Eysenhardt
+
14. Aeginum grimaldii Maas
+ +
15. Solmundella bitentaculata Quoy et Gaimard
+
+
+
Siphonophora 16. Agalma elegans Sars
+
17. Hippopodius hippopus Forskal
+
18. Diphyes chamissonis Huxley
+
+
19. Lensia subtiloides Lens et Van Riemsdijk
+
+
20. Muggiaea atlantica Cunningham
+
21. Chelophyes appendiculata Eschscholtz
+
Ctenophora 22. Pleurobrachia globosa Moser
+
+
+
23. Beroe cucumis Fabricius
+
+
+
Polychaeta 24. Tomopteris pacifica Lzuka
+
25. Pelagobia longicirrata Greeff
+
Cladocera 26. Penilia avirostris Dana
+
27. Evadne tergestina Claus
+
Copepods 28. Calanus sinicus Brodsky
+
+
+
+
29. Canthocalanus pauper Giesbrecht
+
30. Nannocalanus minor Claus
+
31. Eucalanus subcrassus Giesbrecht
+
+
+
+
33. P. aculeatus Giesbrecht
+
+
34. Acrocalanus gracilis Giesbrecht
+
32. Paracalanus parvus Claus
35. A. gibber Giesbrecht
+
+
+
+
+
36. Clausocalanus arcuicornis Dana
+
37. Euchaeta concinna Dana
+
+
+
38. Scolecithrix danae Lubbock
+
+
+
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Table 2 (Continued) Species
Feb.
May
39. Temora turbinate Dana +
41. C. tenuiremis Thompson et Scott
+
+
42. C. dorsispinatus Thompson et Scott
+
43. C. sinensis Chen et Zhang
+
44. C. furcatus Dana
+
45. Sinocalanus tenellus Kikuchi
+
+ +
47. Candacia bradyi A. Scott 48. Labidocera euchaeta Giesbrecht
+ +
+
+
49. L. sinilobata Shen et Lee
+
50. L. detruncate Dana
+
51. Pontella chierchiae Giesbrecht
+
52. P. securifer Brady
+
53. Pontellopsis regalis Dana
+
54. Pontellina plumata Dana +
+
+
+
+
+
+
56. A. danae Giesbrecht
+
+
58. A. negligens Dana 59. Tortanus derjugini Smironov
+
+
55. Acartia pacifica Steuer
57. A. clausi Giesbrecht
Nov.
+
40. Centropages abdominalis Sato
46. Schmackeria poplesia Shen
Aug.
+ +
60. Oithona similis Claus
+
+
61. Oncean sp.
+
62. Clytemnestra scutellata Dana
+
63. Microsetella norvegica Boeck
+
+ +
Mysidacea 64. Acanthomysis brevirostris Wang et Liu
+
65. A. longirostris Ii
+
+
+
Cumacea 66. Diastylis tricincta Zimmer
+
+
+
+
+
+
+
+
+
+
+
+
Amphipoda 67. Tullbergella cuspidata Bovallius 68. Monoculodes limnophilus Tattersall
+
Euphausiacea 69. Pseudeuphausia sinica Wang et Chen Decapoda 70. Acetes chinensis Hansen 71. Acetes sp.
+ +
+
72. Lucifer hanseni Nobili
+
73. Lucifer sp.
+
74. Leptochela gracilis Stimpson
+
75. Latreutes planirostris de Haan
+
+
+
+
Chaetognatha 76. Sagitta enflata Grassi
+
+
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Table 2 (Continued) Species
Feb.
May
Aug.
Nov.
77. S. nagae Alvarino
+
+
+
78. S. bedoti Beraneck
+
+
+
79. S. pulchra Doncaster
+
+
+
Tunicata 80. Oikopleura longicauda Vogt
+
81. Oikopleura dioica Fol
+
82. Oikopleura sp.
+
83. Dolioletta gegenbauri Uljanin
+
84. Dolioletta sp.
+
+
Pelagic mollusca 85. Limacina trochiformis d’Orbigny
+
86. Creseis acicula Rang
+
87. Cavolinia globulosa Rang
+
88. Pneumoderma atlanticum Oken
+
89. Atlanta sp.
+
Pelagic larva 90. Polychaeta larva
+
91. Isopoda larva +
93. Lamellibranchiata larva
+
94. Gastropoda post larva
+
95. Balanus larva
+
+
+
98. Porcellana zoea larva +
100. Palinurus larva
+
+
+
+
+
+
+
+
+
+
+
102. Ophiopluteus larva
+ +
+
104. Engraulis japonicus Temminck et Schlegel
+
+
105. Gobiidae gen. spp.
+
+
most warm water species disappeared, which caused a striking decrease in the population of zooplankton (12 species) and pelagic larvae (3 groups). The seasonal variation of richness of zooplankton species follows the following order: Summer > Spring > Fall > Winter. Eight species of zooplankton were found in all the four seasons (Calanus sinicus, Paracalanus parvus, Labidocera euchaeta, A. Clausi, Diastylis tricincta, Monoculodes limnophilus, Copepod nauplius larva and Brachyura larva). The results showed that besides the water temperature, the variation in the population of copepods, pelagic larvae, and medusae groups was the main reason for the seasonal variation of zooplankton in Sanmen Bay (Table 1).
+
+
101. Squillidae alima larva
103. Clupeidae gen. spp.
+
+
97. Euphausiacea larva
99. Brachyura larva
+
+
92. Cirripedite larva
96. Copepods nauplius larva
+
+
3.1.2 Community structure The zooplankton in Sanmen Bay could be divided into four ecotypes. Coastal low-saline species: This ecotype was the dominant in Sanmen Bay, which accounted for 65% of the total zooplankton species. It was mainly composed of Calanus sinicus, Labidocera euchaeta, Acartia pacifica, Tortanus derjugini, Pseudeuphausia sinica, Sagitta bedoti, and S. nagae. Estuary brackish water species: A low number of estuary brackish water species were identified and they were not found in all the four seasons. It was mainly composed of Schmackeria poplesia, Monoculodes limnophilus, Acanthomysis brevirostris, and A. longirostris.
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Offshore warm water species: Low abundance and a large number of species were two characteristics of the community structure of the offshore warm water species. They entered the bay with the high saline water in summer and fall and played an important role in the community structure of zooplankton in summer. Common species in this group include Euchaeta concinna, Scolecithrix danae, Labidocera detruncate, Pontellina plumat, and Sagitta enflata. Eurytopic species: Only few species of this ecotype were found, which included Paracalanus parvus, Oithona similis, and Dolioletta. 3.2 Seasonal variation of biomass and abundance of zooplankton The average zooplankton biomass for all the four seasons was 171.70 [wet weight] mg/m3, which was higher than that found in Yueqing Bay, China (71.37mg/m3)[7]. The average surface water temperature was 28.4℃ in August. Large number of zooplankton species, especially hydromedusae, was found in such high water temperature, and zooplankton biomass reached an annual maximum (378.31 mg/m3). In contrast, the average water temperature in February was 10.1℃, and only few species were found under such low water temperature. No medusae and Chaetognatha were found. Zooplankton biomass reached an annual minimum of 36.98 mg/m3. Zooplankton biomass was higher in November (138.20 mg/m3) than in May (133.31 mg/ m3) (Fig. 2). The average zooplankton abundance for all the four seasons
Fig. 2 Seasonal variation of biomass and abundance of zooplankton
was 161.80 ind/m3, which was higher than that of Yueqing Bay. The species and abundance of copepods and pelagic larvae increased strikingly in August, which was the reason for the annual maximum of zooplankton abundance (393.68 ind/ m3). In February, because of low water temperature, no warm water species was found and the reproduction rate of zooplankton rapidly decreased, which led to the annual minimum of zooplankton abundance (46.85 ind/m3). Zooplankton abundance was higher in May (153.28 ind/m3) than in November (63.37 ind/m3) (Fig. 2). 3.3 Horizontal distribution of zooplankton biomass In May 2003, the growth rate of zooplankton showed a striking increase. Many species of pelagic larvae, especially large species of medusae, were found, which caused a marked increase in the zooplankton biomass. Zooplankton biomass increased from the upper to the lower bay, and the maximum biomass was found in the middle bay (S12) (Table 3, Fig. 3a). In August 2002, species of zooplankton reached the maximum, including 14 species of medusae. The highest biomass was found in the lower bay, and zooplankton biomass in the upper bay was higher than that in the middle bay (Table 3, Fig. 3b). In November 2002, zooplankton biomass was lower than in August 2002. There was no significant difference in biomass among different parts of Sanmen Bay (Table 3, Fig. 3c). In February 2003, only a few species of zooplankton was found because of the decrease in the warm water species. The medusae were not found in the samples and the biomass was lower than that in the other three seasons. The highest biomass was found in the upper bay, especially at S15 (106.67mg/m3), whereas the biomass in the lower bay was higher than that in the middle bay (Table 3, Fig. 3d). 3.4 Horizontal distribution of zooplankton abundance In May 2003, both species and biomass of pelagic larvae increased along with the increase in the zooplankton abundance. The highest abundance was found in the lower bay (S1, 250 ind/m3). Zooplankton abundance increased from the upper to the lower bay, which followed the horizontal distribution of zooplankton biomass (Table 3, Fig. 4a). In August 2002, more species of pelagic larvae and warm water species were found because of high water temperature. Similar to the biomass, the zooplankton abundance in summer was also higher than those found in the other three seasons and decreased from the upper
Table 3 Seasonal variation of biomass and abundance of zooplankton (Aug. 2002 to May 2003) Abundance (ind/m3)
Biomass (mg/m3) Time
Upper portion
Middle of
Lower portion
of the bay
the bay
of the bay
Mean (mg/m3)
Upper portion of the bay
Middle of the
Lower portion
bay
of the bay
Mean (ind/m3)
May
88.90
126.50
165.40
133.31
125.40
133.50
185.80
153.28
Aug.
284.18
252.20
574.72
378.31
436.86
380.28
347.21
383.68
Nov.
115.12
153.11
140.13
138.20
66.73
59.99
64.06
63.37
Feb.
61.95
17.08
38.16
36.98
90.14
23.68
37.55
46.85
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Fig. 3 Horizontal distribution of zooplankton biomass(mg/m3) (a) May; (b) August; (c) November; (d) February
Fig. 4 Horizontal distribution of zooplankton abundance (ind/m3) (a) May; (b) August; (c) November; (d) February
to the lower bay (Table 3, Fig. 4b). In November 2002, the zooplankton biomass was evenly distributed in Sanmen Bay and significant difference of abundance in different studying areas was not found (Table 3, Fig. 4c). In February 2003, zooplankton abundance reached the minimum (46.85 ind/m3), and the highest abundance was found in S15 (193.33 ind/m3).
Similar to the biomass, the zooplankton abundance increased from the upper to the lower bay (Table 3, Fig. 4d). The relationship between zooplankton and other environmental factors showed that in August, there was a positive regression between zooplankton abundance and total inorganic nitrogen, which were not observed in the other three
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
seasons (Fig. 5a). In February, a positive correlation was found between zooplankton abundance and Chl-a (Fig. 5b). In winter, as the growth rate of phytoplankton and the concentration of Chl-a were very low, the growth and reproduction of zooplankton were limited by phytoplankton biomass. According to the regression analysis, marked relation between zooplankton abundance and environmental factors was not found. 3.5 Seasonal variation of dominant species of zooplankton Coastal low-saline species were the dominant species of zooplankton in Sanmen Bay, especially Calanus sinicus, A. gibber, and Brachyura larva. Different dominant species were found in different seasons with different environmental factors such as water temperature, salinity, and nutrient concentrations (Table 4). In May, the dominant species were Calanus sinicus, L. euchaeta, and Brachyura larva, which accounted for 40% of the total zooplankton abundance, especially in the lower bay where Calanus sinicus and Brachyura larva were abundant. In August, the primary dominant species was A. gibber (100 ind/ m3), constituting 26.05% of the total zooplankton. In addition, high abundance of S. danae, Brachyura larva, and Acanthomysis brevirostris was found in the upper bay. In November, Calanus sinicus was the dominant yet again and was mainly
found in the lower bay, accounting for 20.49% of the total zooplankton abundance. A. gibber and Acartia pacifica were also abundant. In February, the dominant species was Centropages abdominalis (15.32 ind/m3), which was mainly found in the upper bay and accounted for 32.69% of the total zooplankton abundance. Tortanus derjugini and Diastylis tricincta were also the dominant species in February. The seasonal variation of the dominant species of zooplankton was related to the environmental factors such as water temperature and salt concentration. 3.6 Diversity index and evenness index There was a seasonal variation of the zooplankton diversity index in Sanmen Bay. The maximum value of diversity index (3.54) was recorded in August when the number of species (73 species zooplankton and 14 groups of pelagic larvae), abundance, and biomass of zooplankton reached the maximum. The minimum value of diversity index (1.64) was observed in February when the number of species (12 species zooplankton and 3 groups of pelagic larvae), abundance, and biomass of zooplankton reached the minimum. Diversity index in May (3.44) was higher than that in November (3.00). The value of zooplankton evenness index showed the following order: February > May > August > November (Table 5). 3.7 Grazing influence of microzooplankton
Fig. 5 Correlations between zooplankton abundance and environmental parameter (a) Abundance-TIN, Aug. 2002; (b) Abundance-Chl a, Feb. 2003
Table 4 Seasonal variation of dominant species of zooplankton(Aug. 2002 to May 2003) Season
In the percentage of total abundance (%)
Dominant species
May
Calanus sinicus, Labidocera euchaeta, Brachyura larva
August
Acrocalanus gibber, Scolecithrix danae, Brachyura larva
40 42
November
Calanus sinicus, Acrocalanus gibber, Acartia pacifica
42
February
Centropages abdominalis, Tortanus derjugini, Diastylis tricincta
65
Table 5 Seasonal variation of diversity index of zooplankton (Aug. 2002 to May 2003) Season
Diversity index (H′)
Mean of Evenness (J)
Mean
Range
May August
3.44 3.54
2.57–3.97 2.44–4.02
0.79 0.72
November
3.00
2.68–3.26
0.83
February
1.64
0.81–2.65
0.84
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
In recent years, dilution technique has become the most common method for estimating the phytoplankton mortality － rate because of the grazing of microzooplankton[8 12], it was recommended by the Joint Global Ocean Flux Study (JGOFS), and there were several researches on dilution technique in China[7,13]. The results of dilution experiments in this study showed that there was a seasonal variation in grazing rate of microzooplankton, grazing pressure of microzooplankton on phytoplankton, and grazing pressure of microzooplankton on primary production. Growth rate of phytoplankton was higher than grazing rate of microzooplankton in all seasons. In No－ vember 2002, growth rate of phytoplankton (0.89 d 1) reached the maximum value among the four seasons; grazing rate of － zooplankton (0.68 d 1), grazing pressure on phytoplankton －1 － (49.1% d ), and primary production (83.6% d 1) were also the highest among the four seasons. In May 2003, grazing rate － of microzooplankton (0.18 d 1) and grazing pressure of mi－ crozooplankton on phytoplankton (16.1% d 1) reached the minimum value, as growth rate of phytoplankton also reached the minimum, which suggests that grazing rate of microzooplankton might be influenced by the growth rate of phytoplankton. However, minimal effect of microzooplankton － grazing on primary production (58.3% d 1) was observed in August, which was mainly as a result of the high growth rate － of phytoplankton (0.79 d 1) and the low grazing rate of mi－1 crozooplankton (0.38 d ). Recent research showed that 0–75% phytoplankton and 5%–100% primary production were grazed by microzooplankton, which was similar to the results obtained in Sanmen Bay (Table 6, Table 7). Generally, the concentration of Chl-a in phytoplankton was
affected by illumination, nutrition, and water temperature. Growth rate of phytoplankton may be underestimated or overestimated because of cellular fluorescence variation of phytoplankton during the incubation. The community structure of phytoplankton will have an influence on the Chl-a result. To understand the interaction between different nutrient grades in food web of the marine ecosystem, the growth and mortality rates of phytoplankton were simultaneously estimated using the dilution technique and HPLC (High Performance Liquid Chromatography)[14]. In the past decade, there were several reports on the use of flow cytometry in studies on microphytoplankton growth and mortality rates[15,16]. Further research could not be carried out because of restrictions imposed by lack of experiment facilities and conditions.
4
Conclusions
4.1 A total of 89 species of zooplankton belonging to 67 genera and 16 groups of pelagic larvae were found in Sanmen Bay. Copepods were the dominant group with 36 species. The other dominant groups were 23 species of medusae and 16 species of pelagic larvae. There was apparent seasonal variation of zooplankton species caused by water temperature and open seawater invasion. The highest number of zooplankton species was recorded in August. 4.2 Zooplankton in Sanmen Bay could be divided into four ecotypes: coastal low-saline species, estuary brackish water species, offshore warm water species, and eurytopic species. The dominant species were coastal low-saline species, which accounted for 60% of the total zooplankton. There was a sea-
Table 6 Grazing pressure of microzooplankton on phytoplankton and primary production in Sanmen Bay, China (Aug. 2002 to May 2003) Microzooplankton grazing rate (d 1) －
Season
Grazing pressure of microzoo-
Grazing pressure of microzoo-
plankton on phytoplankton
plankton on primary production
(% d 1)
(% d 1) 73.5
－
－
May
0.18
16.1
August
0.38
31.9
58.3
November
0.68
49.1
83.6
February
0.41
33.4
73.7
Table 7 Comparison of results of dilution experiments in different waters of the world Phytoplankton growth rate k
Microzooplankton grazing rate
(d 1) －
(d 1)
0.26–2.07
0.15–0.48
7
1.2–2.0
0.1–1.1
8
Hiroshima Bay, Japan
0.26–1.88
0.20–1.39
9
Monterey Bay, Canada
0.53–1.30
0.23–0.79
10
Fourleague Bay, Louisiana, USA
0.46–2.14
0.32–2.11
11
Western Gulf of St. Lawrence, USA
0.41–1.09
0.34–0.55
12
Bohai Sea, China
0.23–0.73
0.43–0.69
13
Sanmen Bay, China
0.25–0.89
0.18–0.68
This paper
Study area Yueging Bay, China Kaneohe Bay, Hawaii, USA
－
References
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
sonal variation in the dominant species of zooplankton. 4.3 The average zooplankton biomass for all the four seasons was 171.70 mg/m3, and a seasonal variation in the biomass was observed. Zooplankton biomass reached an annual maximum (378.31 mg/m3) in August and an annual minimum (36.98 mg/m3) in February. Zooplankton biomass increased from the upper to the lower bay in May. In August, the maximum biomass was found in the lower bay, and the biomass in the upper bay was higher than the middle bay. In November, there was no significant difference of biomass among different areas of Sanmen Bay. In February, the maximum biomass was found in the upper bay, and the biomass in the lower bay was higher than that in the middle bay. 4.4 The average zooplankton abundance for all the four seasons was 161.80 ind/m3. The abundance reached an annual maximum (383.68 ind /m3) in August and an annual minimum (46.85 ind /m3) in February. Zooplankton abundance increased from the upper to the lower bay in May. In August, zooplankton abundance increased from the lower to the upper bay. In November, there was no significant difference in biomass among different areas of Sanmen Bay. In February, the maximum biomass was found in the upper bay, and the biomass in the lower bay was higher than that in the middle bay. 4.5 There was an obvious seasonal variation in the diversity index of zooplankton in Sanmen Bay, which conformed to the species and abundance of zooplankton. The order of the diversity index was August > May > November > February. Seasonal variation in the evenness index of zooplankton was in the order February > November > May > August. 4.6 There were seasonal variation in the grazing rate of microzooplankton, the growth rate of phytoplankton and the grazing pressure of microzooplankton on phytoplankton and primary production. Grazing rate of microzooplankton was lower than the growth rates of phytoplankton in all the four seasons. In November, growth rate of phytoplankton, grazing rate of microzooplankton, and grazing pressure of microzooplankton on phytoplankton and primary production reached the maximum value of the year. There was a dynamic balance between the grazing pressure of microzooplankton on phytoplankton and the growth rate of phytoplankton.
Acknowledgements We thank Li F, Gao S Q, Zhu G H, Cai Y M., Yang J Y, Peng X, Hao Q, and Wang X G for their technical assistance. Dr. Liu H B, Louisiana University, helped significantly improve this article. This research was supported by the Ocean Development Administration Foundation of Zhejiang Province, China.
References
the coastal zone of Zhejiang Province and its natural resources. Beijing, China: China Ocean Press, 1988. 151–174. [2] Editorial Committee of the Bay Chorography in China. The bay chorography in China. Beijing, China: China Ocean Press, 1992. 5: 291–302. [3] Liu Z S，Wang C S. Distribution and seasonal variation of zooplankton in Sanmen Bay. In: Ning X R et al. Study on the impacts of aquaculture ecosystem and assessment of the aquaculture carrying capacity in Yueqing Bay and Sanmen Bay, China. Beijing, China: China Ocean Press, 2005. 160–168. [4]
State Administration Bureau of Technical Supervision. The specification for oceanographic survey: Marine biology. National Standard of People’s Republic of China GB 12763. 6-91. Beijing, China: China Standardization Press, 1991.
[5] Landry M R, Hassett R P. Estimating the grazing impact of marine microzooplankton. Mar. Biol., 1982, 67: 283–288. [6] Zhang W C, Wang R. Grazing pressure of microzooplankton on phytoplankton and primary production in marine ecosystem. Acta Ecologica Sinica, 2001, 21(8): 1360–1368. [7] Liu Z S, Wang C S, Zhang Z N, et al. Seasonal dynamics and grazing rate of zooplankton in Yueqing Bay. Acta Ecologica Sinica, 2005, 25(8): 1853–1862. [8] Landry M R, Hass L W, Fagerness V L. Dynamics of microbial plankton communities: experiments in Kaneohe Bay, Hawaii. Mar. Ecol. Prog. Ser., 1984, 16: 127–133. [9] Kamiyama T. The impact of grazing by microzooplankton in northern Hiroshima Bay, the Seto Inland Seam, Japan. Mar. Biol., 1994, 119: 77–88. [10] Waterhouse T Y, Welschmeyer N A. Taxon-specific analysis of microzooplankton grazing rates and phytoplankton growth rates. Limnology and Oceanography, 1995, 40: 827– 834. [11]
Dagg M J. Ingestion of phytoplankton by the micro- and mesozooplankton communities in a productive subtropical estuary. J. Plankton Res., 1995, 17: 845–857.
[12] Tamigneaux E, Mingelbier M, Klein B, et al. Grazing by protists and seasonal changes in the size structure of protozooplankton and phytoplankton in a temperate nearshore environment (western Gulf of St. Lawrence, Canada). Mar. Ecol. Prog. Ser., 1997, 146: 231–247. [13] Wang R, Li C, Wang K, et al. Feeding activities of zooplankton in the Bohai Sea. Fishing Oceanography, 1998, 7: 265–271. [14] Latasa M, Landry M R, Schluter L, et al. Pigment-specific growth and grazing rates of phytoplankton in the central equatorial Pacific. Limnology and Oceanography, 1997, 42: 289– 298. [15] Landry M R, Krishtein J, Constantinou J. A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific. Mar. Ecol. Prog. Ser., 1995, 120: 53–63. [16] Liu H B, Suzuki K, Saino T. Phytoplankton growth and microzooplankton grazing in the subarctic Pacific Ocean and the
[1] Editorial Committee of Survey Report on the Coastal Zone of Zhejiang Province and Its Natural Resources. Survey report on
Bering Sea during summer 1999. Deep-Sea Research Part I, 2002, 49: 363–375.
RESEARCH PAPER
Seasonal dynamics of zooplankton and grazing impact of microzooplankton on phytoplankton in Sanmen Bay, China Liu Zhensheng1,2,3, Wang Chunsheng2,3, Zhang Zhinan1, Liu Chenggang2,3, Yang Guanming2 1 College of Marine Life Science, Ocean University of China, Qingdao 266003, China 2 Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China 3 Key Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration, Hangzhou 310012, China
Abstract: The species composition, biomass, abundance and species diversity of zooplankton were determined for samples collected from 12 stations in Sanmen Bay, China, in four cruises from August 2002 to May 2003. Growth of phytoplankton and grazing rates of microzooplankton were measured using the dilution technique. The spatial and temporal variation of zooplankton and its relationship with environmental factors were also analyzed. The results showed that a total of 89 species of zooplankton belonging to 67 genera and 16 groups of pelagic larvae were found in Sanmen Bay. The coastal low-saline species was the dominant ecotype in the study area, and the dominant species were Calanus sinicus, Labidocera euchaeta, Tortanus derjugini, Acartia pacifica, Pseudeuphausia sinica and Sagitta bedoti. Maximum biomass was recorded in August, followed by November and May, and the lowest biomass was recorded in February. Similarly, the highest abundance of zooplankton was observed in August, followed by May, November, and February. Grazing pressure of microzooplankton on phytoplankton in Sanmen Bay existed throughout the year, although the grazing rate of microzooplankton on phytoplankton varied with the season. Estimates for growth rate of phytoplankton －1
ranged from 0.25 d
to 0.89 d 1, whereas grazing rate of microzooplankton ranged between 0.18 d
－1
－
－1
and 0.68 d
in different sea-
sons. The growth rate of phytoplankton exceeded the grazing rate of microzooplankton in all the seasons. Grazing pressure of mi－1
crozooplankton on phytoplankton ranged from 16.1% d production of phytoplankton ranged from 58.3% d
－1
－1
to 49.1% d －1
to 83.6% d
, and the grazing pressure of microzooplankton on primary
in different seasons.
Key Words: zooplankton; biomass; abundance; microzooplankton grazing; Sanmen Bay
1
Introduction
Sanmen Bay is a half-closed bay located on the coast of middle Zhejiang Province, China. The drainage basin of this bay is about 3160 km2, and there are more than 30 streams flowing into the Sanmen Bay. The area of this bay is about 775 km2, and the average water depth is 5–10 m. As one of the most important aquiculture bases of the Zhejiang Province, the Sanmen Bay possesses conducive environmental conditions for the growth of marine plankton. Zooplankton plays a key role in the marine food web. Both the primary production and the aquatic product (fishery) are restricted by variations in the community structure of zooplankton. Furthermore, grazing of
microzooplankton plays an important role in material cycle and energy flow in the marine ecosystem. Since the 1980’s, there have been few studies on zooplankton in the Sanmen Bay. To the best of our knowledge, only few reports have been published thus far on the seasonal variation and grazing － rate of zooplankton in the Sanmen Bay[1 3 ]. This study investigates the community structure, seasonal variations in biomass, abundance, dominant species, diversity index, and grazing rate of zooplankton and discusses the relationship between zooplankton and environmental conditions. The results obtained in this study are useful and significant to evaluate the aquiculture ecosystem in Sanmen Bay, China.
Received date: 2005-09-12; Accepted date 2006-03-10 *Corresponding author. E-mail: [email protected] Copyright © 2006, Ecological Society of China. Published by Elsevier BV. All rights reserved.
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
2
Materials and methods
Four cruises were conducted from August 2002 to May 2003 to investigate the zooplankton population in Sanmen Bay (Fig. 1). Zooplankton samples from 12 stations were collected with vertical hauls of plankton nets (0.505 mm mesh, and 0.50 m mouth diameter) from the bottom to the surface, and then the samples were fixed with 5% formalin in plastic bottles (600 cm3). The biomass of zooplankton was measured and the species were identified at the laboratory following the National Standard of People’s Republic of China [GB 12763.6 -91][4].
Grazing pressure of microzooplankton on phytoplankton was calculated by[6]: Pi = (1-eg) × 100% Grazing pressure of microzooplankton on primary production was calculated by[6]: Pp = [ek-e(k-g)]/(ek-1) × 100% Diversity index and evenness index were calculated using the formulae of Shannon-Weaver and Pielou: S
H ′ = −∑( Pi )log 2 ( Pi ) i =1
J = H ′ / log 2 S Where Pi is the ratio between the species of one kind of plankton and the total species of plankton, and S is the number of species. The Sanmen Bay was divided into three zones: upper bay (S14, S15, S16), middle bay (S7, S9, S12, S18), and lower bay (S1, S2, S3, S5, S10).
3
Fig. 1 Investigation stations in Sanmen Bay, China
Grazing rates of microzooplankton were measured using the dilution technique developed by Landry and Hassett[5], in which samples were collected at the beginning and the end of the experiment for concentration of chlorophyll a. Replicate dilution treatments of 0.25, 0.5, 0.75, and 1.0× natural seawater were prepared in polycarbonate bottles. Measured amounts of water, which was filtered using the GF/F glassfiber membrane, was added to the experimental bottles; subsequently, the bottles were gently filled and mixed with unfiltered seawater. The water samples used for the dilution experiments were collected from middle of Sanmen Bay. The grazing rates of the microzooplankton were calculated by: Pt = Po e(k-dg)t Where Pt and Po are the final and the initial existing stock of phytoplankton, respectively, k is the growth rate of the phytoplankton, g the grazing rate of the microzooplankton, and d the dilution[6].
Results and discussion
3.1 Composition and community structure of zooplankton species 3.1.1 Species composition A total of 89 species of zooplankton, belonging to 67 genera and 16 groups of pelagic larvae, were found in Sanmen Bay. Copepods were found to be the dominant group among the zooplankton, with 36 species of this group being identified. In addition, species of pelagic larvae (16), Hydromedusae (15), Siphonophora (6), Decapoda (6), Tunicata (5), Pelagic mollusca (5), Chaetognatha (4), Ctenophora (2), Polychaeta (2), Cladocera (2), Mysidacea (2), Amphipoda (2), Cumacea (1), and Euphausiacea (1) were also identified (Table 1, Table 2). All groups of zooplankton in Sanmen Bay showed a marked seasonal variation. Most species of zooplankton were found in August when high water temperature and the invasion of offshore seawater were observed, resulting in an increase of warm water species and offshore species. Seventy-three species of zooplankton and 14 groups of pelagic larvae were found, including 48 species of copepods and medusae. A greater number of species of zooplankton were found in May (33 species of zooplankton and 12 groups of pelagic larvae) than in November (31 species of zooplankton and 5 groups of pelagic larvae), which was mainly because of medusae and pelagic larva. With a decrease in water temperature in February,
Table 1 Zooplankton composition and seasonal variation in Sanmen Bay, China (Aug. 2002 to May 2003) Time
Group Copepods
Medusae
Pelagic larva
Other groups
3
2
15
3
12
7
45
21
4
14
25
87
4
4
5
8
36
Feb. 2003
10
May 2003
16
7
Aug. 2002
23
Nov. 2002
15
Chaetognatha
Total
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Table 2 Species of zooplankton in Sanmen Bay, China (Aug. 2002 to May 2003) Species
Feb.
May
Aug.
Nov.
Hydromedusae 1. Sarsia nipponica Uchida
+
2. Ectopleura sp.
+
3. Euphysa aurata Forbes
+
4. Turritopsis nutricula McCrady
+
5. Clytia hemisphaericum Linnaeus
+
6. Obelia spp.
+
7. Phialucium sp.
+
8. Octophialucium indicum Kramp
+
9. Eirene ceylonensis Browne
+
10. Eutima (Otorchis) gegenbauri Haechel
+
11. Aequorea conica Browne
+
12. Aeginum sp.
+
13. Liriope tetraphylla Chamisso et Eysenhardt
+
14. Aeginum grimaldii Maas
+ +
15. Solmundella bitentaculata Quoy et Gaimard
+
+
+
Siphonophora 16. Agalma elegans Sars
+
17. Hippopodius hippopus Forskal
+
18. Diphyes chamissonis Huxley
+
+
19. Lensia subtiloides Lens et Van Riemsdijk
+
+
20. Muggiaea atlantica Cunningham
+
21. Chelophyes appendiculata Eschscholtz
+
Ctenophora 22. Pleurobrachia globosa Moser
+
+
+
23. Beroe cucumis Fabricius
+
+
+
Polychaeta 24. Tomopteris pacifica Lzuka
+
25. Pelagobia longicirrata Greeff
+
Cladocera 26. Penilia avirostris Dana
+
27. Evadne tergestina Claus
+
Copepods 28. Calanus sinicus Brodsky
+
+
+
+
29. Canthocalanus pauper Giesbrecht
+
30. Nannocalanus minor Claus
+
31. Eucalanus subcrassus Giesbrecht
+
+
+
+
33. P. aculeatus Giesbrecht
+
+
34. Acrocalanus gracilis Giesbrecht
+
32. Paracalanus parvus Claus
35. A. gibber Giesbrecht
+
+
+
+
+
36. Clausocalanus arcuicornis Dana
+
37. Euchaeta concinna Dana
+
+
+
38. Scolecithrix danae Lubbock
+
+
+
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Table 2 (Continued) Species
Feb.
May
39. Temora turbinate Dana +
41. C. tenuiremis Thompson et Scott
+
+
42. C. dorsispinatus Thompson et Scott
+
43. C. sinensis Chen et Zhang
+
44. C. furcatus Dana
+
45. Sinocalanus tenellus Kikuchi
+
+ +
47. Candacia bradyi A. Scott 48. Labidocera euchaeta Giesbrecht
+ +
+
+
49. L. sinilobata Shen et Lee
+
50. L. detruncate Dana
+
51. Pontella chierchiae Giesbrecht
+
52. P. securifer Brady
+
53. Pontellopsis regalis Dana
+
54. Pontellina plumata Dana +
+
+
+
+
+
+
56. A. danae Giesbrecht
+
+
58. A. negligens Dana 59. Tortanus derjugini Smironov
+
+
55. Acartia pacifica Steuer
57. A. clausi Giesbrecht
Nov.
+
40. Centropages abdominalis Sato
46. Schmackeria poplesia Shen
Aug.
+ +
60. Oithona similis Claus
+
+
61. Oncean sp.
+
62. Clytemnestra scutellata Dana
+
63. Microsetella norvegica Boeck
+
+ +
Mysidacea 64. Acanthomysis brevirostris Wang et Liu
+
65. A. longirostris Ii
+
+
+
Cumacea 66. Diastylis tricincta Zimmer
+
+
+
+
+
+
+
+
+
+
+
+
Amphipoda 67. Tullbergella cuspidata Bovallius 68. Monoculodes limnophilus Tattersall
+
Euphausiacea 69. Pseudeuphausia sinica Wang et Chen Decapoda 70. Acetes chinensis Hansen 71. Acetes sp.
+ +
+
72. Lucifer hanseni Nobili
+
73. Lucifer sp.
+
74. Leptochela gracilis Stimpson
+
75. Latreutes planirostris de Haan
+
+
+
+
Chaetognatha 76. Sagitta enflata Grassi
+
+
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Table 2 (Continued) Species
Feb.
May
Aug.
Nov.
77. S. nagae Alvarino
+
+
+
78. S. bedoti Beraneck
+
+
+
79. S. pulchra Doncaster
+
+
+
Tunicata 80. Oikopleura longicauda Vogt
+
81. Oikopleura dioica Fol
+
82. Oikopleura sp.
+
83. Dolioletta gegenbauri Uljanin
+
84. Dolioletta sp.
+
+
Pelagic mollusca 85. Limacina trochiformis d’Orbigny
+
86. Creseis acicula Rang
+
87. Cavolinia globulosa Rang
+
88. Pneumoderma atlanticum Oken
+
89. Atlanta sp.
+
Pelagic larva 90. Polychaeta larva
+
91. Isopoda larva +
93. Lamellibranchiata larva
+
94. Gastropoda post larva
+
95. Balanus larva
+
+
+
98. Porcellana zoea larva +
100. Palinurus larva
+
+
+
+
+
+
+
+
+
+
+
102. Ophiopluteus larva
+ +
+
104. Engraulis japonicus Temminck et Schlegel
+
+
105. Gobiidae gen. spp.
+
+
most warm water species disappeared, which caused a striking decrease in the population of zooplankton (12 species) and pelagic larvae (3 groups). The seasonal variation of richness of zooplankton species follows the following order: Summer > Spring > Fall > Winter. Eight species of zooplankton were found in all the four seasons (Calanus sinicus, Paracalanus parvus, Labidocera euchaeta, A. Clausi, Diastylis tricincta, Monoculodes limnophilus, Copepod nauplius larva and Brachyura larva). The results showed that besides the water temperature, the variation in the population of copepods, pelagic larvae, and medusae groups was the main reason for the seasonal variation of zooplankton in Sanmen Bay (Table 1).
+
+
101. Squillidae alima larva
103. Clupeidae gen. spp.
+
+
97. Euphausiacea larva
99. Brachyura larva
+
+
92. Cirripedite larva
96. Copepods nauplius larva
+
+
3.1.2 Community structure The zooplankton in Sanmen Bay could be divided into four ecotypes. Coastal low-saline species: This ecotype was the dominant in Sanmen Bay, which accounted for 65% of the total zooplankton species. It was mainly composed of Calanus sinicus, Labidocera euchaeta, Acartia pacifica, Tortanus derjugini, Pseudeuphausia sinica, Sagitta bedoti, and S. nagae. Estuary brackish water species: A low number of estuary brackish water species were identified and they were not found in all the four seasons. It was mainly composed of Schmackeria poplesia, Monoculodes limnophilus, Acanthomysis brevirostris, and A. longirostris.
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Offshore warm water species: Low abundance and a large number of species were two characteristics of the community structure of the offshore warm water species. They entered the bay with the high saline water in summer and fall and played an important role in the community structure of zooplankton in summer. Common species in this group include Euchaeta concinna, Scolecithrix danae, Labidocera detruncate, Pontellina plumat, and Sagitta enflata. Eurytopic species: Only few species of this ecotype were found, which included Paracalanus parvus, Oithona similis, and Dolioletta. 3.2 Seasonal variation of biomass and abundance of zooplankton The average zooplankton biomass for all the four seasons was 171.70 [wet weight] mg/m3, which was higher than that found in Yueqing Bay, China (71.37mg/m3)[7]. The average surface water temperature was 28.4℃ in August. Large number of zooplankton species, especially hydromedusae, was found in such high water temperature, and zooplankton biomass reached an annual maximum (378.31 mg/m3). In contrast, the average water temperature in February was 10.1℃, and only few species were found under such low water temperature. No medusae and Chaetognatha were found. Zooplankton biomass reached an annual minimum of 36.98 mg/m3. Zooplankton biomass was higher in November (138.20 mg/m3) than in May (133.31 mg/ m3) (Fig. 2). The average zooplankton abundance for all the four seasons
Fig. 2 Seasonal variation of biomass and abundance of zooplankton
was 161.80 ind/m3, which was higher than that of Yueqing Bay. The species and abundance of copepods and pelagic larvae increased strikingly in August, which was the reason for the annual maximum of zooplankton abundance (393.68 ind/ m3). In February, because of low water temperature, no warm water species was found and the reproduction rate of zooplankton rapidly decreased, which led to the annual minimum of zooplankton abundance (46.85 ind/m3). Zooplankton abundance was higher in May (153.28 ind/m3) than in November (63.37 ind/m3) (Fig. 2). 3.3 Horizontal distribution of zooplankton biomass In May 2003, the growth rate of zooplankton showed a striking increase. Many species of pelagic larvae, especially large species of medusae, were found, which caused a marked increase in the zooplankton biomass. Zooplankton biomass increased from the upper to the lower bay, and the maximum biomass was found in the middle bay (S12) (Table 3, Fig. 3a). In August 2002, species of zooplankton reached the maximum, including 14 species of medusae. The highest biomass was found in the lower bay, and zooplankton biomass in the upper bay was higher than that in the middle bay (Table 3, Fig. 3b). In November 2002, zooplankton biomass was lower than in August 2002. There was no significant difference in biomass among different parts of Sanmen Bay (Table 3, Fig. 3c). In February 2003, only a few species of zooplankton was found because of the decrease in the warm water species. The medusae were not found in the samples and the biomass was lower than that in the other three seasons. The highest biomass was found in the upper bay, especially at S15 (106.67mg/m3), whereas the biomass in the lower bay was higher than that in the middle bay (Table 3, Fig. 3d). 3.4 Horizontal distribution of zooplankton abundance In May 2003, both species and biomass of pelagic larvae increased along with the increase in the zooplankton abundance. The highest abundance was found in the lower bay (S1, 250 ind/m3). Zooplankton abundance increased from the upper to the lower bay, which followed the horizontal distribution of zooplankton biomass (Table 3, Fig. 4a). In August 2002, more species of pelagic larvae and warm water species were found because of high water temperature. Similar to the biomass, the zooplankton abundance in summer was also higher than those found in the other three seasons and decreased from the upper
Table 3 Seasonal variation of biomass and abundance of zooplankton (Aug. 2002 to May 2003) Abundance (ind/m3)
Biomass (mg/m3) Time
Upper portion
Middle of
Lower portion
of the bay
the bay
of the bay
Mean (mg/m3)
Upper portion of the bay
Middle of the
Lower portion
bay
of the bay
Mean (ind/m3)
May
88.90
126.50
165.40
133.31
125.40
133.50
185.80
153.28
Aug.
284.18
252.20
574.72
378.31
436.86
380.28
347.21
383.68
Nov.
115.12
153.11
140.13
138.20
66.73
59.99
64.06
63.37
Feb.
61.95
17.08
38.16
36.98
90.14
23.68
37.55
46.85
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
Fig. 3 Horizontal distribution of zooplankton biomass(mg/m3) (a) May; (b) August; (c) November; (d) February
Fig. 4 Horizontal distribution of zooplankton abundance (ind/m3) (a) May; (b) August; (c) November; (d) February
to the lower bay (Table 3, Fig. 4b). In November 2002, the zooplankton biomass was evenly distributed in Sanmen Bay and significant difference of abundance in different studying areas was not found (Table 3, Fig. 4c). In February 2003, zooplankton abundance reached the minimum (46.85 ind/m3), and the highest abundance was found in S15 (193.33 ind/m3).
Similar to the biomass, the zooplankton abundance increased from the upper to the lower bay (Table 3, Fig. 4d). The relationship between zooplankton and other environmental factors showed that in August, there was a positive regression between zooplankton abundance and total inorganic nitrogen, which were not observed in the other three
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
seasons (Fig. 5a). In February, a positive correlation was found between zooplankton abundance and Chl-a (Fig. 5b). In winter, as the growth rate of phytoplankton and the concentration of Chl-a were very low, the growth and reproduction of zooplankton were limited by phytoplankton biomass. According to the regression analysis, marked relation between zooplankton abundance and environmental factors was not found. 3.5 Seasonal variation of dominant species of zooplankton Coastal low-saline species were the dominant species of zooplankton in Sanmen Bay, especially Calanus sinicus, A. gibber, and Brachyura larva. Different dominant species were found in different seasons with different environmental factors such as water temperature, salinity, and nutrient concentrations (Table 4). In May, the dominant species were Calanus sinicus, L. euchaeta, and Brachyura larva, which accounted for 40% of the total zooplankton abundance, especially in the lower bay where Calanus sinicus and Brachyura larva were abundant. In August, the primary dominant species was A. gibber (100 ind/ m3), constituting 26.05% of the total zooplankton. In addition, high abundance of S. danae, Brachyura larva, and Acanthomysis brevirostris was found in the upper bay. In November, Calanus sinicus was the dominant yet again and was mainly
found in the lower bay, accounting for 20.49% of the total zooplankton abundance. A. gibber and Acartia pacifica were also abundant. In February, the dominant species was Centropages abdominalis (15.32 ind/m3), which was mainly found in the upper bay and accounted for 32.69% of the total zooplankton abundance. Tortanus derjugini and Diastylis tricincta were also the dominant species in February. The seasonal variation of the dominant species of zooplankton was related to the environmental factors such as water temperature and salt concentration. 3.6 Diversity index and evenness index There was a seasonal variation of the zooplankton diversity index in Sanmen Bay. The maximum value of diversity index (3.54) was recorded in August when the number of species (73 species zooplankton and 14 groups of pelagic larvae), abundance, and biomass of zooplankton reached the maximum. The minimum value of diversity index (1.64) was observed in February when the number of species (12 species zooplankton and 3 groups of pelagic larvae), abundance, and biomass of zooplankton reached the minimum. Diversity index in May (3.44) was higher than that in November (3.00). The value of zooplankton evenness index showed the following order: February > May > August > November (Table 5). 3.7 Grazing influence of microzooplankton
Fig. 5 Correlations between zooplankton abundance and environmental parameter (a) Abundance-TIN, Aug. 2002; (b) Abundance-Chl a, Feb. 2003
Table 4 Seasonal variation of dominant species of zooplankton(Aug. 2002 to May 2003) Season
In the percentage of total abundance (%)
Dominant species
May
Calanus sinicus, Labidocera euchaeta, Brachyura larva
August
Acrocalanus gibber, Scolecithrix danae, Brachyura larva
40 42
November
Calanus sinicus, Acrocalanus gibber, Acartia pacifica
42
February
Centropages abdominalis, Tortanus derjugini, Diastylis tricincta
65
Table 5 Seasonal variation of diversity index of zooplankton (Aug. 2002 to May 2003) Season
Diversity index (H′)
Mean of Evenness (J)
Mean
Range
May August
3.44 3.54
2.57–3.97 2.44–4.02
0.79 0.72
November
3.00
2.68–3.26
0.83
February
1.64
0.81–2.65
0.84
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
In recent years, dilution technique has become the most common method for estimating the phytoplankton mortality － rate because of the grazing of microzooplankton[8 12], it was recommended by the Joint Global Ocean Flux Study (JGOFS), and there were several researches on dilution technique in China[7,13]. The results of dilution experiments in this study showed that there was a seasonal variation in grazing rate of microzooplankton, grazing pressure of microzooplankton on phytoplankton, and grazing pressure of microzooplankton on primary production. Growth rate of phytoplankton was higher than grazing rate of microzooplankton in all seasons. In No－ vember 2002, growth rate of phytoplankton (0.89 d 1) reached the maximum value among the four seasons; grazing rate of － zooplankton (0.68 d 1), grazing pressure on phytoplankton －1 － (49.1% d ), and primary production (83.6% d 1) were also the highest among the four seasons. In May 2003, grazing rate － of microzooplankton (0.18 d 1) and grazing pressure of mi－ crozooplankton on phytoplankton (16.1% d 1) reached the minimum value, as growth rate of phytoplankton also reached the minimum, which suggests that grazing rate of microzooplankton might be influenced by the growth rate of phytoplankton. However, minimal effect of microzooplankton － grazing on primary production (58.3% d 1) was observed in August, which was mainly as a result of the high growth rate － of phytoplankton (0.79 d 1) and the low grazing rate of mi－1 crozooplankton (0.38 d ). Recent research showed that 0–75% phytoplankton and 5%–100% primary production were grazed by microzooplankton, which was similar to the results obtained in Sanmen Bay (Table 6, Table 7). Generally, the concentration of Chl-a in phytoplankton was
affected by illumination, nutrition, and water temperature. Growth rate of phytoplankton may be underestimated or overestimated because of cellular fluorescence variation of phytoplankton during the incubation. The community structure of phytoplankton will have an influence on the Chl-a result. To understand the interaction between different nutrient grades in food web of the marine ecosystem, the growth and mortality rates of phytoplankton were simultaneously estimated using the dilution technique and HPLC (High Performance Liquid Chromatography)[14]. In the past decade, there were several reports on the use of flow cytometry in studies on microphytoplankton growth and mortality rates[15,16]. Further research could not be carried out because of restrictions imposed by lack of experiment facilities and conditions.
4
Conclusions
4.1 A total of 89 species of zooplankton belonging to 67 genera and 16 groups of pelagic larvae were found in Sanmen Bay. Copepods were the dominant group with 36 species. The other dominant groups were 23 species of medusae and 16 species of pelagic larvae. There was apparent seasonal variation of zooplankton species caused by water temperature and open seawater invasion. The highest number of zooplankton species was recorded in August. 4.2 Zooplankton in Sanmen Bay could be divided into four ecotypes: coastal low-saline species, estuary brackish water species, offshore warm water species, and eurytopic species. The dominant species were coastal low-saline species, which accounted for 60% of the total zooplankton. There was a sea-
Table 6 Grazing pressure of microzooplankton on phytoplankton and primary production in Sanmen Bay, China (Aug. 2002 to May 2003) Microzooplankton grazing rate (d 1) －
Season
Grazing pressure of microzoo-
Grazing pressure of microzoo-
plankton on phytoplankton
plankton on primary production
(% d 1)
(% d 1) 73.5
－
－
May
0.18
16.1
August
0.38
31.9
58.3
November
0.68
49.1
83.6
February
0.41
33.4
73.7
Table 7 Comparison of results of dilution experiments in different waters of the world Phytoplankton growth rate k
Microzooplankton grazing rate
(d 1) －
(d 1)
0.26–2.07
0.15–0.48
7
1.2–2.0
0.1–1.1
8
Hiroshima Bay, Japan
0.26–1.88
0.20–1.39
9
Monterey Bay, Canada
0.53–1.30
0.23–0.79
10
Fourleague Bay, Louisiana, USA
0.46–2.14
0.32–2.11
11
Western Gulf of St. Lawrence, USA
0.41–1.09
0.34–0.55
12
Bohai Sea, China
0.23–0.73
0.43–0.69
13
Sanmen Bay, China
0.25–0.89
0.18–0.68
This paper
Study area Yueging Bay, China Kaneohe Bay, Hawaii, USA
－
References
LIU Zhensheng et al. / Acta Ecologica Sinica, 2006, 26(12): 3931–3941
sonal variation in the dominant species of zooplankton. 4.3 The average zooplankton biomass for all the four seasons was 171.70 mg/m3, and a seasonal variation in the biomass was observed. Zooplankton biomass reached an annual maximum (378.31 mg/m3) in August and an annual minimum (36.98 mg/m3) in February. Zooplankton biomass increased from the upper to the lower bay in May. In August, the maximum biomass was found in the lower bay, and the biomass in the upper bay was higher than the middle bay. In November, there was no significant difference of biomass among different areas of Sanmen Bay. In February, the maximum biomass was found in the upper bay, and the biomass in the lower bay was higher than that in the middle bay. 4.4 The average zooplankton abundance for all the four seasons was 161.80 ind/m3. The abundance reached an annual maximum (383.68 ind /m3) in August and an annual minimum (46.85 ind /m3) in February. Zooplankton abundance increased from the upper to the lower bay in May. In August, zooplankton abundance increased from the lower to the upper bay. In November, there was no significant difference in biomass among different areas of Sanmen Bay. In February, the maximum biomass was found in the upper bay, and the biomass in the lower bay was higher than that in the middle bay. 4.5 There was an obvious seasonal variation in the diversity index of zooplankton in Sanmen Bay, which conformed to the species and abundance of zooplankton. The order of the diversity index was August > May > November > February. Seasonal variation in the evenness index of zooplankton was in the order February > November > May > August. 4.6 There were seasonal variation in the grazing rate of microzooplankton, the growth rate of phytoplankton and the grazing pressure of microzooplankton on phytoplankton and primary production. Grazing rate of microzooplankton was lower than the growth rates of phytoplankton in all the four seasons. In November, growth rate of phytoplankton, grazing rate of microzooplankton, and grazing pressure of microzooplankton on phytoplankton and primary production reached the maximum value of the year. There was a dynamic balance between the grazing pressure of microzooplankton on phytoplankton and the growth rate of phytoplankton.
Acknowledgements We thank Li F, Gao S Q, Zhu G H, Cai Y M., Yang J Y, Peng X, Hao Q, and Wang X G for their technical assistance. Dr. Liu H B, Louisiana University, helped significantly improve this article. This research was supported by the Ocean Development Administration Foundation of Zhejiang Province, China.
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